Abstract
Watermelon (Citrullus lanatus) is an important horticultural crop worldwide, but peel cracking caused by peel hardness severely decreases its quality. Lignification is one of the important functions of class III peroxidase (PRX), and its accumulation in the plant cell wall leads to cell thickening and wood hardening. For in-depth physiological and genetical understanding, we studied the relationship between peel hardness and lignin accumulation and the role of PRXs affecting peel lignin biosynthesis using genome-wide bioinformatics analysis. The obtained results showed that lignin accumulation gradually increased to form the peel stone cell structure, and tissue lignification led to peel hardness. A total of 79 ClPRXs (class III) were identified using bioinformatics analysis, which were widely distributed on 11 chromosomes. The constructed phylogenetics indicated that ClPRXs were divided into seven groups and eleven subclasses, and gene members of each group had highly conserved intron structures. Repeated pattern analysis showed that deletion and replication events occurred during the process of ClPRX amplification. However, in the whole-protein sequence alignment analysis, high homology was not observed, although all contained four conserved functional sites. Repeated pattern analysis showed that deletion and replication events occurred during ClPRXs’ amplification process. The prediction of the promoter cis-acting element and qRT-PCR analysis in four tissues (leaf, petiole, stem, and peel) showed different expression patterns for tissue specificity, abiotic stress, and hormone response by providing a genetic basis of the ClPRX gene family involved in a variety of physiological processes in plants. To our knowledge, we for the first time report the key roles of two ClPRXs in watermelon peel lignin synthesis. In conclusion, the extensive data collected in this study can be used for additional functional analysis of ClPRXs in watermelon growth and development and hormone and abiotic stress response.
Highlights
The class III peroxidase gene family (PRXs) is a widely distributed isozyme family type that is well known to have various short names, e.g., PRX, POD, POX, and PER, and contributes to multiple significant physiological reactions in plants [1]
When constructing the evolutionary tree with the Arabidopsis PRX gene family, we found that genes of group II and III ClPRX members had evolutionary relationship changes and showed a scattered distribution
Previous studies have found a homology of total amino acid sequences of PRX gene family members in multiple specimens of less than 35% [5,27], but due to its coding region and motif research, we found that high similarity, indicating a relatively conserved status, was present in a number of structural domains, including the heme binding site distal histidine (Hd) and proximal histidine (HP)
Summary
The class III peroxidase gene family (PRXs) is a widely distributed isozyme family type that is well known to have various short names, e.g., PRX, POD, POX, and PER, and contributes to multiple significant physiological reactions in plants [1]. The proteins formed by these genes exhibit highly conserved amino acid motifs that include two conserved histidine motifs with chemical binding sites for heme, distal histidine vital for catalytic activity, and eight cysteines that interact to form constant disulfide bonds and are essential amino acids in the secondary structure of peroxidases [11]. The amino acid sequences of all these genes are highly conserved, and the protein structure and molecular weight are similar between the lineal and adjacent homologous genes; the presence of multiple catalytic forms of peroxidases suggests that these peroxidases may be functional in specialized forms [12]. Genome-wide analysis of these polygene families would be very helpful to better understand their gene composition and the characteristics of the protein structure, as well as to explain the relationship between differential peroxidase genes and physiological characteristics
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