Phylogenetic analysis of pectin-related gene families in Physcomitrella patensand nine other plant species yields evolutionary insights into cell walls

Abstract

BackgroundPectins are acidic sugar-containing polysaccharides that are universally conserved components of the primary cell walls of plants and modulate both tip and diffuse cell growth. However, many of their specific functions and the evolution of the genes responsible for producing and modifying them are incompletely understood. The moss Physcomitrella patens is emerging as a powerful model system for the study of plant cell walls. To identify deeply conserved pectin-related genes in Physcomitrella, we generated phylogenetic trees for 16 pectin-related gene families using sequences from ten plant genomes and analyzed the evolutionary relationships within these families.ResultsContrary to our initial hypothesis that a single ancestral gene was present for each pectin-related gene family in the common ancestor of land plants, five of the 16 gene families, including homogalacturonan galacturonosyltransferases, polygalacturonases, pectin methylesterases, homogalacturonan methyltransferases, and pectate lyase-like proteins, show evidence of multiple members in the early land plant that gave rise to the mosses and vascular plants. Seven of the gene families, the UDP-rhamnose synthases, UDP-glucuronic acid epimerases, homogalacturonan galacturonosyltransferase-like proteins, β-1,4-galactan β-1,4-galactosyltransferases, rhamnogalacturonan II xylosyltransferases, and pectin acetylesterases appear to have had a single member in the common ancestor of land plants. We detected no Physcomitrella members in the xylogalacturonan xylosyltransferase, rhamnogalacturonan I arabinosyltransferase, pectin methylesterase inhibitor, or polygalacturonase inhibitor protein families.ConclusionsSeveral gene families related to the production and modification of pectins in plants appear to have multiple members that are conserved as far back as the common ancestor of mosses and vascular plants. The presence of multiple members of these families even before the divergence of other important cell wall-related genes, such as cellulose synthases, suggests a more complex role than previously suspected for pectins in the evolution of land plants. The presence of relatively small pectin-related gene families in Physcomitrella as compared to Arabidopsis makes it an attractive target for analysis of the functions of pectins in cell walls. In contrast, the absence of genes in Physcomitrella for some families suggests that certain pectin modifications, such as homogalacturonan xylosylation, arose later during land plant evolution.

Functional Characterization of UDP-apiose Synthases from Bryophytes and Green Algae Provides Insight into the Appearance of Apiose-containing Glycans during Plant Evolution

“…Because we could not detect wall-bound apiose even in P. patens lines overexpressing SpUAS, it is probable that the apiosyltransferases required for the synthesis of RG-II and ApiGalA do not exist in bryophytes or green algae. It is notable that phylogenetic analyses of pectin-related gene families in P. patens suggest that this moss lacks homologs of vascular plant xylogalacturonan xylosyltransferases and rhamnogalacturonan I arabinosyltransferases (52). Thus, expanding the repertoire of cell wall pectin structures may have accompanied the transition from avascular to vascular plants.…”

Can mosses serve as model organisms for forest research?

“…In addition, the genes responsible for the biosynthesis and modification of the cell wall component pectin share a common ancestor in mosses and vascular plants (McCarthy et al 2014). In order to protect the early land plants from UV radiation, secondary metabolism diversified and phenylpropanoid metabolism emerged (Weng and Chapple 2010).…”

Evolution of the cell wall components during terrestrialization

“…Pectins are abundant already in CGA, occurring even in single-celled ones, as Penium margaritaceum [49,112]. The presence of pectin in the ancestors of land plants suggests they importance for the expansion of land or at least for the development of first non-vascular land plants, which contain much more pectins than more evolutionarily advanced vascular plants.…”

“…In seed plants, three main groups of pectins are distinguished: homogalacturonan (HG), rhamnogalacturonan I (RG-I) and rhamnogalacturonan II (RG-II) [113]. Sometimes, as the fourth separate group, the xylogalacturonans (XGA) are also given [112,115].…”

“…The most important seems to be the regulation of cell adhesion [110,111], which is essential for the development and functioning of multicellular organisms, as land plants. Pectins participate also in the apical and diffusive growth of cells [112], are involved in the defense response against pathogens [113] and regulate the cell wall strengthening [114]. In seed plants, three main groups of pectins are distinguished: homogalacturonan (HG), rhamnogalacturonan I (RG-I) and rhamnogalacturonan II (RG-II) [113].…”