A comparative analysis of the evolution, expression, and cis-regulatory element of polygalacturonase genes in grasses and dicots

Abstract

Cell walls are a distinguishing characteristic of plants essential to their survival. The pectin content of primary cell walls in grasses and dicots is distinctly different. Polygalacturonases (PGs) can degrade pectins and participate in multiple developmental processes of plants. This study comprehensively compared the evolution, expression, and cis-regulatory element of PGs in grasses and dicots. A total of 577 PGs identified from five grasses and five dicots fell into seven clades. Evolutionary analysis demonstrated the distinct differences between grasses and dicots in patterns of gene duplication and loss, and evolutionary rates. Grasses generally contained much fewer clade C and F members than dicots. We found that this disparity was the result of less duplication and more gene losses in grasses. More duplications occurred in clades D and E, and expression analysis showed that most of clade E members were expressed ubiquitously at a high overall level and clade D members were closely related to male reproduction in both grasses and dicots, suggesting their biological functions were highly conserved across species. In addition to the general role in reproductive development, PGs of clades C and F specifically played roles in root development in dicots, shedding light on organ differentiation between the two groups of plants. A regulatory element analysis of clade C and F members implied that possible functions of PGs in specific biological responses contributed to their expansion and preservation. This work can improve the knowledge of PGs in plants generally and in grasses specifically and is beneficial to functional studies.

Genome-Wide Identification and Analysis of Polygalacturonase Genes in Solanum lycopersicum

“…Domains I and II may constitute catalytic sites, domain III may participate in the reaction, and domain IV constitutes a possible candidate for the interaction with the ionic groups of the carboxylic acid groups in the substrate [9]. Domain III shows lower conservation and is missing in PGs belonging to clade E, and a PG gene can be identified as containing at least one of the four conserved domains [7,8,9,29]. Of the 54 PGs, 40 contained four conserved domains (Figure 1, Table 1).…”

“…In B. rapa and C. sativus , most BrPG and CsPG genes in Clade E were found to be ubiquitously expressed in different tissues [8,12]. Expression patterns of PG genes in the other two dicots ( Glycine max and Medicago truncatula ) and two grasses ( Zea mays and O. sativa ) also showed that most of the clade E members could be detected at high overall expression levels in all tissues [7]. In accordance with previous research, we found that more than half SlPGs of Group I belonged to Clade E and were also defined as being expressed ubiquitously (Figure 4, Table S3) which further proved the previous theory that the Clade E members of PG family are possibly ancient proteins and are fundamental and indispensable in almost all plant organs of different species [7,10].…”

“…Expression patterns of PG genes in the other two dicots ( Glycine max and Medicago truncatula ) and two grasses ( Zea mays and O. sativa ) also showed that most of the clade E members could be detected at high overall expression levels in all tissues [7]. In accordance with previous research, we found that more than half SlPGs of Group I belonged to Clade E and were also defined as being expressed ubiquitously (Figure 4, Table S3) which further proved the previous theory that the Clade E members of PG family are possibly ancient proteins and are fundamental and indispensable in almost all plant organs of different species [7,10]. The PG genes of Clades C, D, and F may be associated with flower development, and the main expression pattern of PGs in clades C and F may be different between the grasses and dicots [7,9,10,12].…”

“…Studies have reported that PGs are encoded by a large gene family, and the evolution of plant PG gene family has been explored by many researchers [7]. Up to now, the expression patterns of 75, 53, 46, 68, 99, and 85 PG genes in Populus , Cucumis sativus , Oryza sativa , Arabidopsis thaliana , Brassica rapa and Malus × domestica have been respectively investigated [8,9,10,11,12].…”

“…Additionally, a total of 577 PGs have been identified from five grasses and five dicots. In addition, the evolution, expression, and cis -regulatory element of them were comprehensively compared [7]. Although most PG genes function in vegetative growth, there are some fruit-specific PG genes acting on the development and maturation of the fruit as well as the formation of abscission zone in fruit stalks after fruit ripening [2,13].…”