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. 2022 Jun 20:13:943184.
doi: 10.3389/fpls.2022.943184. eCollection 2022.

Genome-Wide Comprehensive Survey of the Subtilisin-Like Proteases Gene Family Associated With Rice Caryopsis Development

Kaifeng Zheng  1 , Lu Pang  1 , Xiuhua Xue  1 , Ping Gao  1 , Heping Zhao  1 , Yingdian Wang  1   2 , Shengcheng Han  1   2
Affiliations

Genome-Wide Comprehensive Survey of the Subtilisin-Like Proteases Gene Family Associated With Rice Caryopsis Development

Kaifeng Zheng et al. Front Plant Sci. .

Abstract

Subtilisin-like proteases (SUBs), which are extensively distributed in three life domains, affect all aspects of the plant life cycle, from embryogenesis and organogenesis to senescence. To explore the role of SUBs in rice caryopsis development, we recharacterized the OsSUB gene family in rice (Oryza sativa ssp. japonica). In addition, investigation of the SUBs was conducted across cultivated and wild rice in seven other Oryza diploid species (O. brachyantha, O. glaberrima, O. meridionalis, O. nivara, O. punctata, O. rufipogon, and O. sativa ssp. indica). Sixty-two OsSUBs were identified in the latest O. sativa ssp. japonica genome, which was higher than that observed in wild species. The SUB gene family was classified into six evolutionary branches, and SUB1 and SUB3 possessed all tandem duplication (TD) genes. All paralogous SUBs in eight Oryza plants underwent significant purifying selection. The expansion of SUBs in cultivated rice was primarily associated with the occurrence of tandem duplication events and purifying selection and may be the result of rice domestication. Combining the expression patterns of OsSUBs in different rice tissues and qRT-PCR verification, four OsSUBs were expressed in rice caryopses. Moreover, OsSUBs expressed in rice caryopses possessed an earlier origin in Oryza, and the gene cluster formed by OsSUBs together with the surrounding gene blocks may be responsible for the specific expression of OsSUBs in caryopses. All the above insights were inseparable from the continuous evolution and domestication of Oryza. Together, our findings not only contribute to the understanding of the evolution of SUBs in cultivated and wild rice but also lay the molecular foundation of caryopsis development and engineering improvement of crop yield.

Keywords: Oryza; expression in rice caryopsis; gene family; rice; subtilisin-like proteases.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Identification and phylogenetic relationships of SUBs in eight Oryza species. (A) Comparison of the number of SUB gene family members in eight Oryza. The red section of the heatmap reflects the number variation of SUBs on twelve chromosomes. The blue portion of the heatmap visualizes the number of SUBs within the six clades. The height of the bars and the shade of the color indicate the size of the numbers. (B) An abbreviated evolutionary tree clearly shows the six primary separated groups and is labeled with different color backgrounds. (C) After performing alignment of 477 subtilases protein sequences, a phylogenetic tree of SUBs was produced using the neighbor-joining method. According to the classification, the branches of different clades are indicated by various colors, and the bootstrap values are noted at each branch node.
Figure 2
Figure 2
Chromosome distribution, duplication, and colinearity of SUB genes in rice. Diagram of twelve chromosomes of O. sativa ssp. japonica is depicted, and 62 OsSUBs are mapped to the chromosomes. Tandem duplications are shown using a red curve, and blue lines connect genes, which hold a collinearity relationship. The heatmap on the chromosome roughly depicts the rice chromosome gene density.
Figure 3
Figure 3
Adaptive evolutionary profiles correspond to the SUB gene family in Oryza. (A) Overall average of the SUB family in eight species by the Coden-Based Z-test. (B–D) Value of p matrix for positive selection, purifying selection, and neutral selection. We considered p < 0.05 to indicate significant selection. In each Oryza plant, percentages indicate the extent to which significantly selected loci account for the total.
Figure 4
Figure 4
Detailed information on the phylogenetic relationships, protein domains and gene structures of OsSUBs. (A) Phylogenetic tree of the 62 SUB proteins in O. sativa ssp. japonica. The N-J tree of OsSUBs is colored using the color scheme in Figure 1C, and the bootstrap values are indicated at the branch nodes. (B) Conserved functional structural domains of OsSUB proteins. (C) The horizontal black line, yellow box and green box indicate the position of introns, CDS, and UTR, respectively. The scale bar below shows the nucleotide length of 18,000 bp.
Figure 5
Figure 5
Tissue-specific expression of the OsSUB gene. (A) Expression patterns of the OsSUB gene family in different rice tissues and developmental stages. The scale indicating the relative signal strength values is displayed on the right side of the heatmap (Log Scale: Base = 2; LogWith = 1). Genes with tandem duplication relationships are linked to each other with red lines. (B–F) The expression profiles of four OsSUBs and OsASP1 were determined using quantitative real-time polymerase chain reaction (qRT–PCR) in CPBs at 0, 3, 5, and 12 days after heading (DAH; CPB-0, −3, −5, and −12) and CSBs at 0, 3, 5, and 12 DAH (CSB-0, −3, −5, and −12). We performed three independent biological replicates, and OsActin3 was used as an internal control.
Figure 6
Figure 6
Synteny history of the SUB gene family and genomes of Oryza. The Oryza phylogenetic profile was combined with a synteny relationship map of the whole genome of eight Oryza species. Synteny relationships between the genomes of two neighboring species are depicted in gray, and magenta indicates the orthologous gene pairs. The orthologous genes to four genes (OsSUBs29, OsSUBs53, OsSUBs58, OsSUB63) are presented in pink, blue, yellow and green, respectively.
Figure 7
Figure 7
PhyloView of several OsSUB reference genes in the rice genome. Phylogenetic species tree of the reference gene is shown on the left. On the right, the reference genes and their homologous copies in other Oryza plants are in the center surrounded by their neighboring genes. Homologue genes are colored using the same color. A–D Show the PhyloViews of the four genes OsSUBs29, OsSUBs53, OsSUBs58, and OsSUB63, which were identified as the reference genes in O. sativa ssp. japonica, respectively.
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