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Article

MIKC-Type MADS-Box Gene Family Discovery and Evolutionary Investigation in Rosaceae Plants

by
Yue Qin
1,2,
Gaopu Zhu
1,
Fangdong Li
1,
Lin Wang
1,
Chen Chen
1 and
Han Zhao
1,*
1
Research Institute of Non-Timber Forestry Chinese Academy of Forestry, Zhengzhou 450003, China
2
College of Forestry, Nanjing Forestry University, Nanjing 210037, China
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(7), 1695; https://doi.org/10.3390/agronomy13071695
Submission received: 24 April 2023 / Revised: 21 June 2023 / Accepted: 22 June 2023 / Published: 25 June 2023
(This article belongs to the Special Issue Flowering and Flower Development in Plants)
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Abstract

:
MADS-box is an important transcriptional regulatory element in plant growth. The MIKC-type MADS-box genes play important roles. However, the identification and evolutionary investigation of MIKC-type MADS-box family members in Rosaceae have been inadequate. Therefore, based on whole-genome data from Prunus dulcis, Prunus salicina, Prunus armeniaca, Prunus persica, Prunus mira, and Amygdalus nana, we depicted the evolution and divergence patterns of MIKC-type MADS-box family genes. In this study, we found 222 MIKC-type MADS-box genes from six Rosaceae species. These genes were classified into five clades, and only motif 1 was identified across all MIKC-type MADS-box proteins, except PdMADS42 and PmiMADS16. The structural properties of these genes significantly varied in sequence lengths between species, despite the high levels of similarity in exon lengths and numbers. MIKC-type MADS-box genes were found to have mostly been limited through purifying selection processes. Remarkably divergent regions were found inside the MIKC-type MADS-box genes’ domains, where clade III displayed more conserved activities and may have retained more original functions over the evolutionary process; clade I, on the other hand, may have undergone substantial functional limitations in a specific functional role. These findings provide the groundwork for future research into the molecular evolutionary processes of the plant MIKC-type MADS-box gene family.

1. Introduction

Flower organs are the basis of plant evolution and classification, and have always played important roles in plant development and biological research [1]. The MADS-box gene family is a class of transcription factors widely distributed among animals, plants, fungi, and other organisms [2,3]. MADS-box derives its name from the first initials of fore groups of genes: the mini chromosome maintenance 1 genes from yeast (MCM1), the agamous genes from Arabidopsis Thaliana (AG), deficiens genes from snapdragon (DEF), and serum response factor genes from humans (SRF). These genes all contain a MADS-box conserved region of about 180 bp at the N-terminal, while identifying the similar DNA sequences [4,5]. The plant MADS-box genes were discovered from the mutant study of the model plants Arabidopsis and Snapdragon. MADS-box genes are widely distributed throughout the genome and expressed at different development stages. Their functions are involved in all aspects of plant growth and development, especially the development and regulation of flower organs, including initiation, differentiation, morphogenesis, and gene transcription regulation, and have become some of the most relevant transcription factor family in plants [6]. The MADS-box gene family in plants can be divided into Type I and Type II. Due to the relatively simple structure and functional redundancy of Type I genes, studies on plant MADS-box genes mostly focus on Type II genes, also known as MIKC-type genes [1]. The encoded protein consists of four domains: MADS domain, I domain (intervening domain), K domain (keratin-like domain), and C-terminal domain. [7]. The MADS-box domain and region I are associated with the formation of protein dimers, the K-box domain mediates protein interactions, and the C-terminal is associated with transcription factor activation and the formation of higher-order protein complexes [8,9].
With the development of sequencing technology and bioinformatics, more and more plants have been thoroughly studied through genome or transcriptome sequencing. Many MADS-box gene family members and their functions within the flower organs of various species have been identified and revealed, including genes controlling flowering time and flowering inhibition (FLC, SVP, SOC1, AGL24), genes regulating floral meristem differentiation (CAL and FUL), and genes governing floral organ characteristics [10,11,12,13]. The pathway controlling flowering initiation and the genes involved, response pathway, and expression regulation mechanism were also analyzed. For example, overexpression of BpAP1 gene in European silver birch can cause early flowering [14], while overexpression of PvMADS5, a SEP homologous gene in bamboo, causes delayed flowering in Arabidopsis plants [15]. These studies have improved understanding of the MADS-box gene family, but many members are yet to be discovered, and the regulation mechanism of flower organ development requires further research.
Prunus dulcis, Prunus salicina, Prunus armeniaca, Prunus persica, Prunus mira, and Amygdalus nana are important economic forestry species in Rosaceae. The study of genes related to flower regulation is of great value not only in phylogeny and taxonomy, but also in genetic improvement and cultivation techniques. In previous studies, researchers have conducted the identification and function analysis of the MADS-box gene family in Prunus persica, Prunus armeniaca, and Prunus dulcis, obtaining a number of genes, illustrating the genes’ structure and sequence features, and analyzing the gene functions. However, studies investigating its evolution between different species are limited. Thus, in this study, we used genome-wide data of six Rosaceae plant species (Prunus dulcis, Prunus salicina, Prunus armeniaca, Prunus persica, Prunus mira, and Amygdalus nana) to screen for MIKC-type MADS-box gene family members. We also looked at the evolutionary relationship, areas of functional divergence, and amino acid structures of the discovered MIKC-type MADS-box genes. These findings are not only important for elucidating the adaptive history of the Rosaceae species, but also for predicting the functional area of the MIKC-type MADS-box genes.

2. Materials and Methods

2.1. Gene Family Identification

Genomic sequence and annotation data for Prunus dulcis, Prunus salicina, Prunus armeniaca, Prunus persica, and Prunus mira were obtained from the GDR database (rosaceae.org), and the Amygdalus nana genome assembly was obtained through our research facility (private information). We utilized the sequences of Arabidopsis MADS-box proteins as a search basis to retrieve MIKC-type MADS-box proteins, employing the local alignment searching modality (BLASTP) with an E value of 1 × 10−10 [16,17]. Then, HMMER v3.3.2 with the hidden Markov model (HMM) profile (PF00319 and PF01486) was employed to explore the proteomes with parameters ‘hmmsearch—notextw—acc—cut_ga_’ [18]. Next, we compared the MADS-box domain using SMART (smart.embl.de) with the Pfam database in the normal smart mode.

2.2. Sequence Analysis

We used MAFFT 7.310 with parameters ‘mafft—maxiterate 1000—globalpair input > output’ to perform multiple protein sequence alignment [19]. The conserved motifs of the MIKC-type MADS-box proteins were investigated using the MEME Suite 5.5.0 with parameters ‘meme julei_6_species. fasta—protein—oc.—nostatus—time 14,400—mod anr—nmotifs 10—minw 6—maxw 100—objfun classic—markov_order 0′ [20]. WebLogo 2.8.2 was used to display the sequences [21], and Tbtools software v1.106 was used to visualize the MEME and gene structure results.

2.3. Phylogenetic and Conservative Analyses

ProtTest 3.4 with model ‘LG + I + G + F’ was used to construct the optimum protein substitution model [22]. Using the neighbor-joining technique and MEGA Version 10.2.2 software, we built a phylogenetic tree using JTT + G with 1000 bootstrap repetitions [23]. Then, we used R-ggtree software 1.8.1 to enhance the phylogenetic tree [24,25,26].

2.4. Selective Evolutionary Pressure Analysis

The Codeml program EasyCodeml Version 1.4 was used to analyze the selective evolutionary pressure at the branch, site, and branch-site models (BM, SM, and BSM, respectively) [27]. Branch models are used to identify the adaptive development of several branches. Site models can discover the ω ratio between the sites and positive selected sites. Provided that the ω ratio varies between the sites and branches, BSMs may be used [28,29,30,31].

2.5. Functional Difference Analyses

The DIVERGE 3.0 tool was used to analyze the functional divergences and distance of the gene family members [32]. Type-I mutations result from functional deviations following gene duplication, subsequently causing distinct evolutionary rates to be shown by duplicate genes. The residues in duplicate genes that showed striking variations in amino acid properties across copies tested using type-II functional divergences [33,34]. Clusters i and j had a type-I functional distance equal to dF(i,j) = −ln(1 − θij). Wang and Gu proved that the dF is additive under a scenario of independence, such that the functional branch dimension for a given gene cluster x is bF(x), and the functional branch dimension of clusters i and j is bF(i) plus bF(j). In the case of a known ij, the cluster branch of the functional branch length may be calculated using the normal least squares technique; if bF = 0, then the duplicate site of the gene has evolved at a pace very close to that of the ancestor gene [35].

3. Results

3.1. Phylogenetic and Sequence Analyses

We identified 222 MIKC-type MADS-box proteins from six Rosaceae species’ whole genome data. Of those identified, 54, 27, 23, 69, 23, and 26 MIKC-type MADS-box genes could be detected in Prunus dulcis (PdMADS1-54), Prunus salicina (PsMADS1-27), Prunus armeniaca (PaMADS1-23), Prunus persica (PpMADS1-69), Prunus mira (PmiMADS1-23), and Amygdalus nana (AnMADS1-26), respectively. The amino acid lengths ranged from 162 aa to 670 aa.
Phylogenetic analysis revealed five distinct groups (clades I–V) within the MIKC-type MADS-box gene family. There was a significant difference in the number of genes across the five clades, with the largest and smallest clades (clade I and III) having 110 and 6, respectively (Table 1, Figure 1). The six species’ genes were found in nearly every clade. The genes of Prunus dulcis and Prunus persica were the most abundant in clades I, IV and V. Prunus persica had most genes in clade II, but Prunus armeniaca was missing. The six species had the same amount of genes in clade III (Table 1, Figure 2). The results suggested that the MIKC-type MADS-box genes in Rosaceae are nearly identical, but serve distinct purposes.

3.2. Motif and Structure Analyses

Ten conserved motifs, ranging from 21 to 80 amino acids, were found in this investigation. Only Motif 1 was found in all of the MIKC-type MADS-box proteins (Figure 3), except PdMADS42 and PmiMADS16. Furthermore, MIKC-type MADS-box proteins had substantially identical sequences for 10 amino acid residues (alanine, cysteine, glutamic acid, glycine, lysine, leucine, glutamine, arginine, serine, and threonine) (Figure 4). On the other hand, some MIKC-type MADS-box proteins lacked certain motifs; for example, Motifs 1 and 6 did not exist in PmiMADS16, and Motifs 4 and 6 did not exist in AnMADS23. However, there were similar or identical arrangement orders and motif types within the same clades. The results showed that the six Rosaceae species’ MIKC-type MADS-box proteins were relatively conserved within a specific clade; the structural analysis produced similar results.
The results of the exon-intron structure analysis showed that the amino acid lengths ranged from 163 to 671. Among them, PsMADS3, PsMADS4, PsMADS7, PsMADS8, and PsMADS24 had no introns (Figure 5). The remaining MIKC-type MADS-box genes had 2–42 exon and 1–41 intron structures. Genes with 8 exons accounted for 47.75 percent of the total (106/222), most genes contained 7 or 8 exons, and only one gene contained 42 exons. This proves that the structures are specialized after gene duplication. These genes also have somewhat complicated architectures, including lengthy initial exons. In conclusion, the conserved motifs, gene architectures, and evolutionary connections of the MIKC-type MADS-box proteins were quite similar. Additionally, the diversification of gene roles was suggested due to the differences in the retained motifs and gene architectures among clades.

3.3. Selective Pressure Analysis

We used EasyCodeML to analyze the selective pressure, used the branch model to test the evolutionary rate difference, and used the branch-site model to increase the detection of positive selection sites in the foreground branches. The results showed that the genetic differentiation had no significant differences (p > 0.05), and no positive sites were obtained according to the branch model and branch-site model results (Table 2 and Table 3). Thus, we assumed the same selection pressure for each point and used the site model for testing the selection site positivity in these sequences. We found that most sites were subjected to purifying and neutral selections, and only the M8 model identified one site as having a significant positive selection site (Table 4). Although we obtained the positive selection sites, the MIKC-type MADS-box genes mainly underwent purifying selection events.

3.4. Functional Divergence Analysis

Gene families comprise multiple homologous genes with similar structures but different functions. In order to see whether changes in amino acid sequences within the MIKC-type MADS-box genes led to adaptive functional variation, we investigated the functional divergence of five distinct groups. The results suggest that, except for clades I/V, most type I coefficient θ values across the clades were statistically > 0, which indicates the presence of type I functional divergences across the clades. Six clades (I/II, I/III, II/III, II/IV, III/IV, and III/V) were remarkable (p < 0.001) for type I functional divergence. Clades III/V had the highest functional divergence coefficient θ (= 1.150), whereas clades I/V had the lowest (=−0.002). Other clades’ type I θ values also varied, indicating that their rates of evolution were unique. In addition, type I functionally divergent sites were not detected in clades I/II, I/V, II/V, III/V, and IV/V (Table 5).

3.5. Functional Distance Analysis

Type I functional divergence-related cluster analyses were unable to determine which groups of duplicated genes were hampered by functional bottlenecks. Therefore, we compared the bF values across the five clades and found that they changed, indicating that unique roles evolved in the MIKC-type MADS-box gene family throughout time. Furthermore, the MIKC-type MADS-box genes tended to be conserved, as shown by bF values above 0. The lowest bF value (−2.453) was found in clade III, suggesting that the functions of the genes in this clade were more conserved and may have kept more of their original forms during evolution. With the longest functional branch length (0.405), clade I likely underwent considerable alterations to its functional restrictions in order to fulfill its specialized functional purpose (Table 6).

4. Discussion

The MADS-box gene family plays an essential role in plant reproductive growth, and it also provides a research hotspot. However, most studies on the MADS-box gene family in Rosaceae mainly focus on identification and functional analysis in only one species [36,37,38,39]. In order to understand the variation pattern of MADS-box gene structure and function among different species, our study performed MIKC-type MADS-box gene identification between six key species in Rosaceae, and investigated their evolutionary relationship. These results are of great significance in understanding the MADS-box family function.
In the present study, we identified 222 MIKC-type MADS-box genes within six Rosaceae species. Among them, there were 54, 27, 23, 69, 23, and 26 genes in Prunus dulcis, Prunus salicina, Prunus armeniaca, Prunus persica, Prunus mira, and Amygdalus nana, respectively, which was almost consistent with other findings in Rosaceae [36,37]. However, the number of MIKC-type MADS-box family members was quite different from other families. For instance, comparing with 232 members in legumes (92 genes in Glycine max, 45 genes in Medicago truncatula, 50 genes in Vitis vinifera, and 45 genes in Arabidopsis thaliana), the number was generally smaller in Rosaceae [40]. In the studies of conserved motifs and structure analysis, we found that no motif was shared by all MIKC-type MADS-box proteins, however Motif 1 was shared by almost all proteins, with the exception of PdMADS42 and PmiMADS16. These results suggested that Motif 1 was conserved across members of this gene family, and that PdMADS42 and PmiMADS16 had distinct purposes. Additionally, different species had varied sequence lengths, although the exon number and length were highly similar. Identified from Prunus salicina, the PsMADS3, PsMADS4, PsMADS7, PsMADS8, and PsMADS24 had no introns, and the gene annotation did not determine the intron structure. The result showed that intron-involving alleles or inversion might have deleted these introns due to homologous recombination, after the reverse transcription of mature mRNA [41].
Phylogenetic analysis revealed five distinct clades within the MIKC-type MADS-box gene family of the six Rosaceae species. The six species genes could be found in almost every clade, but Prunus armeniaca did not exist in clade II. The results showed that the six species could not be distinguished by them, and the genes in clade II might have some special functions which were missing in Prunus armeniaca. According to previous research, we found that Prunus armeniaca had some differences in the phenotypic characteristics of its flowers and fruit compared with the other five species. For instance, the petal was round-to-obovate, and the calyx tube was cylindrical with short fluff at base; moreover, the florescence and fruit stage were relatively early in Prunus armeniaca [42]. With further analysis and verification, we may be able to obtain several specific genes associated with these traits.
Using three models (branch, branch-site, and site models) to perform selective pressure analysis of the six species, we obtained only one positive site in the site model, and there were no positive sites in the branch and branch-site models. It suggested that various places undergo various selection forces, but the evolution and function of MIKC-type MADS-box genes were conserved, and purifying selection limited the MIKC-type MADS-box gene family in Rosaceae [43,44]. Inadequate site-related positive selection data may have been eliminated because they were reduced by the vast majority of the remainder of sites being under the evolutionary condition of neutral or purifying selection [45]. In addition, we found the results of the branch and branch-site models indicated no significant differences, which might be due to the six species being sibling species, or the conformity of the genomes and annotation level among the six species; nevertheless, further analysis is required to clearly understand the reasons.
Functional divergence analysis may be utilized to outline the putative residues of amino acids that cause the functional diversification of gene families, which occurs as a result of gene duplication. In this investigation, we found Type I functionality was shown to vary significantly among clades, and obtained locations that had functional divergence (Q(k) > 0.90). It suggested that the functional divergence of the current Rosaceae gene family was mostly attributable to the differing proportions of evolution following genetic duplications. In addition, members of clade III kept more of their original roles throughout evolution, whereas those of clade I specialized theirs to serve a specific purpose. In future, we can research the gene functions of clade I to analyze their different functions throughout their evolution.
In order to better study the gene mutations in Rosaceae, our research facility has assembled the genome-wide sequence of Amygdalus nana for the first time. Amygdalus nana is a treasured wild species of the Tertiary period deciduous forests in the ancient Mediterranean [46]. At present, there are only several natural populations in China, Kazakhstan, and Russia, which are listed as endangered plants in China [47]. The kernel of Amygdalus nana, a vital species of non-timber forestry, has an oil content of 51.1%, similar to that of almond and higher than that of oil crops, such as rapeseed, cottonseed, and soybean [48]. In addition, having a strong ability to adapt to an extremely harsh environment, especially with cold and drought tolerance, it can grow in the hilly and mountainous areas at −35 °C and annual precipitation of 50mm. Therefore, further research on Amygdalus nana may shed light on the evolution of and relationships between Rosaceae species.

5. Conclusions

In this study, the evolution of MIKC-type MADS-box gene family members in six Rosaceae plants was analyzed for the first time. 222 MIKC-type MADS-box family genes were identified from Prunus dulcis, Prunus salicina, Prunus armeniaca, Prunus persica, Prunus mira, and Amygdalus nana. The results of sequence and phylogenetic analyses showed that these genes were divided into five groups, the six species genes could be found in almost every clade, but Prunus armeniaca did not exist in clade II. Using selective evolutionary pressure and functional difference analyses, a number of positive selection sites and functional divergence locations were obtained. In addition, the conservation between different clades was evaluated, and it was concluded that the genes of clade I were specialized to serve a specific purpose. These results provide great help in the further mining of functional genes for key traits.

Author Contributions

Formal analysis, Y.Q., L.W. and C.C.; data curation, Y.Q., F.L. and H.Z.; writing—original draft preparation, Y.Q. and G.Z.; writing—review and editing, H.Z. and F.L.; visualization, L.W. and C.C.; project administration, H.Z. and G.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Key Research and Development Program of Xinjiang Uygur Autonomous Region (2022292937) and the National Key Research and Development Program of China (2022YFD2200400).

Data Availability Statement

Required data might be provided following a proper request from the senior author.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. NJ phylogenetic tree of the MIKC-type MADS-box gene family from Prunus mira (PmiMADS), Prunus armeniaca (PaMADS), Prunus persica (PpMADS), Prunus dulcis (PdMADS), Prunus salicina (PsMADS), and Amygdalus nana (AnMADS) in Rosaceae plants. Blue is clade I, green is II, purple is III, light blue is IV, and pink is V.
Figure 1. NJ phylogenetic tree of the MIKC-type MADS-box gene family from Prunus mira (PmiMADS), Prunus armeniaca (PaMADS), Prunus persica (PpMADS), Prunus dulcis (PdMADS), Prunus salicina (PsMADS), and Amygdalus nana (AnMADS) in Rosaceae plants. Blue is clade I, green is II, purple is III, light blue is IV, and pink is V.
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Agronomy 13 01695 g002 550
Figure 2. The distribution of MIKC-type MADS-box genes from six Rosaceae species in different clades. Species are represented by different colored boxes.
Figure 2. The distribution of MIKC-type MADS-box genes from six Rosaceae species in different clades. Species are represented by different colored boxes.
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Agronomy 13 01695 g003 550
Figure 3. The conserved motifs of 222 MIKC-type MADS-box family members. Motifs 1 to 10 are represented by different colored boxes.
Figure 3. The conserved motifs of 222 MIKC-type MADS-box family members. Motifs 1 to 10 are represented by different colored boxes.
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Agronomy 13 01695 g004 550
Figure 4. Sequence logo of Motif 1. Amino acid residues are represented by different colored letters.
Figure 4. Sequence logo of Motif 1. Amino acid residues are represented by different colored letters.
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Agronomy 13 01695 g005 550
Figure 5. Gene structure of 222 MIKC-type MADS-box gene family members. The green boxes represent exons, and the gray lines represent introns.
Figure 5. Gene structure of 222 MIKC-type MADS-box gene family members. The green boxes represent exons, and the gray lines represent introns.
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Table
Table 1. The MIKC-type MADS-box genes of six Rosaceae species.
Table 1. The MIKC-type MADS-box genes of six Rosaceae species.
SpeciesCommon NameMIKC-Type MADS-Box Gene NumbersClade
IIIIIIIVV
Amygdalus nanaShort almond26143117
Prunus miraLight walnut23113126
Prunus persicaPeach692691528
Prunus armeniacaApricot23150125
Prunus salicinaPlum27143127
Prunus dulcisAlmond543031713
Total 2221102161966
Table
Table 2. Branch model parameters of selective pressure analysis.
Table 2. Branch model parameters of selective pressure analysis.
Modelnp/aaln LParameters EstimatesCompared Modelp-Value
Two ratio Model 2448−3172.993ω:ω0 = 1.533ω1 = 0.768; ω2 = 999.000; ω3 = 0.862; ω4 = 2.208;
ω5 = 2.452		Model 0
vs.
Two ratio Model 2		>0.05
Model 0443−3175.884ω=1.558
Table
Table 3. Branch-site model parameters of selective pressure analysis.
Table 3. Branch-site model parameters of selective pressure analysis.
Modelnp/aaln LParameters EstimatesCompared Modelp-ValuePositive Sites
Model A446−3166.858Site class012a2bModel A
vs. Model A null		>0.05Not allowed
f0.0000.0000.1560.844
ω00.2291.0000.2291.000
ω10.2291.000999.000999.000
Model A null445−3165.2061 Not allowed
Table
Table 4. Site model parameters of selective pressure analysis.
Table 4. Site model parameters of selective pressure analysis.
Modelnpln LParameters EstimatesCompared Modelp-ValuePositive Selected Sites
M0443−3144.848ω = 0.318M0 vs. M3<0.001Not allowed
M3447−3054.877p: 0.266, 0.519, 0.216 Not allowed
ω: 0.095, 0.432, 0.955
M1a444−3071.511p: 0.330, 0.670M1a vs. M2a<0.001Not allowed
ω: 0.193, 1.000
M2a446−3062.176p: 0.289, 0.528, 0.183 Not allowed
ω: 0.204, 1.000, 2.045
M7444−3055.573p = 0.760, q = 1.042M7 vs. M8>0.05Not allowed
M8446−3053.688p0 = 0.778 11 E 0.616
p = 0.852
Table
Table 5. Functional divergence analysis of MIKC-type MADS gene family in Rosaceae.
Table 5. Functional divergence analysis of MIKC-type MADS gene family in Rosaceae.
Cladeθ ± SEMFE
z-Scores		p-ValueAmino Acid Position with Q(k) > 0.9
Type IType IIType IType II
I/II0.579 ± 0.156−0.112 ±0.189−4.115715<0.001>0.05—
I/III0.871 ± 0.1580.005 ± 0.182−6.191108<0.001>0.05193,299,307,316.332,341,343, 346,359,370,371,374,386,397,400,403,407
I/IV0.327 ± 0.225−0.081 ± 0.207−1.505518>0.001>0.05190,301,302,310,311,316.346,349.361,
388,403
I/V−0.002 ± 0.263−0.660 ± 0.3790.009046>0.001>0.05—
II/III1.058 ± 0.1590.299 ± 0.050−7.305373<0.001>0.05190,192,193,195,272,273,290,292,295,
297,298,299,300,301,303,305,307,314,
316,318,320,321,332,342,343,345,347,
349,356,358,359,366,370,371,373,374,
385,386,387,395,396,397,403,404,405,
406,409,411
II/IV0.874 ± 0.2390.193 ± 0.070−3.826513<0.001>0.05193,271,272,290,296,298,299,301,302,
305,310,311,313,316,319,320,331,341,
347,350,352,361,370,371,373,382,388,
394,397,403,409
II/V0.831 ± 0.288−0.221 ± 0.203−2.974702>0.001>0.05—
III/IV1.085 ± 0.2320.232 ± 0.063−4.882459<0.001>0.05190,193,195,271,292,296,301,302,307,
310,311,313,314,319,321,331,332,341,
343,345,347,349,350,352,358,359,361,
374,382,386,387,388,394,395,404,406
III/V1.150 ± 0.279−0.233 ± 0.205−4.220686<0.001>0.05—
IV/V0.205 ± 0.410−0.425 ± 0.248−0.50314>0.001>0.05—
Table
Table 6. Type I functional distance analysis of MIKC-type MADS gene family in Rosaceae.
Table 6. Type I functional distance analysis of MIKC-type MADS gene family in Rosaceae.
CladebF
I0.405
II−1.270
III−2.453
IV−0.801
V−0.403
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Qin, Y.; Zhu, G.; Li, F.; Wang, L.; Chen, C.; Zhao, H. MIKC-Type MADS-Box Gene Family Discovery and Evolutionary Investigation in Rosaceae Plants. Agronomy 2023, 13, 1695. https://doi.org/10.3390/agronomy13071695

AMA Style

Qin Y, Zhu G, Li F, Wang L, Chen C, Zhao H. MIKC-Type MADS-Box Gene Family Discovery and Evolutionary Investigation in Rosaceae Plants. Agronomy. 2023; 13(7):1695. https://doi.org/10.3390/agronomy13071695

Chicago/Turabian Style

Qin, Yue, Gaopu Zhu, Fangdong Li, Lin Wang, Chen Chen, and Han Zhao. 2023. "MIKC-Type MADS-Box Gene Family Discovery and Evolutionary Investigation in Rosaceae Plants" Agronomy 13, no. 7: 1695. https://doi.org/10.3390/agronomy13071695

APA Style

Qin, Y., Zhu, G., Li, F., Wang, L., Chen, C., & Zhao, H. (2023). MIKC-Type MADS-Box Gene Family Discovery and Evolutionary Investigation in Rosaceae Plants. Agronomy, 13(7), 1695. https://doi.org/10.3390/agronomy13071695

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