The Cell Wall Proteome of Marchantia polymorpha Reveals Specificities Compared to Those of Flowering Plants

Abstract

Primary plant cell walls are composite extracellular structures composed of three major classes of polysaccharides (pectins, hemicelluloses, and cellulose) and of proteins. The cell wall proteins (CWPs) play multiple roles during plant development and in response to environmental stresses by remodeling the polysaccharide and protein networks and acting in signaling processes. To date, the cell wall proteome has been mostly described in flowering plants and has revealed the diversity of the CWP families. In this article, we describe the cell wall proteome of an early divergent plant, Marchantia polymorpha, a Bryophyte which belong to one of the first plant species colonizing lands. It has been possible to identify 410 different CWPs from three development stages of the haploid gametophyte and they could be classified in the same functional classes as the CWPs of flowering plants. This result underlied the ability of M. polymorpha to sustain cell wall dynamics. However, some specificities of the M. polymorpha cell wall proteome could be highlighted, in particular the importance of oxido-reductases such as class III peroxidases and polyphenol oxidases, D-mannose binding lectins, and dirigent-like proteins. These proteins families could be related to the presence of specific compounds in the M. polymorpha cell walls, like mannans or phenolics. This work paves the way for functional studies to unravel the role of CWPs during M. polymorpha development and in response to environmental cues.

Developmental Plasticity of the Amphibious Liverwort Riccia fluitans

“…In the liverwort M. polymorpha , the Mp SBG9 transcription factor is a key regulator of cuticle biosynthesis and controls surface permeability ( Xu et al, 2021 ). Additionally, lineage-specific compounds contribute to adaptive cell wall remodeling processes, as revealed by recent M. polymorpha cell wall proteome analyses ( Kolkas et al, 2021 ). It was also shown that angiosperms can adapt surface layers in response to an altered environment.…”

“…A large diversity of cell wall polymers and cuticle compounds contributed to cope with variable, often limited water availability ( Sørensen et al, 2010 ; Philippe et al, 2020 ). The production of cuticular waxes in M. polymorpha is affected by growth conditions, which together with cell wall polymer diversity likely contributed to the adaptation to terrestrial habitats ( Kolkas et al, 2021 ; Xu et al, 2021 ).…”

N-glycoproteins in Plant Cell Walls: A Survey

“…Several plants have been studied: Marchantia polymorpha [ 52 ] as an early divergent plant; Zea mays [ 34 ], Triticum aestivum [ 33 ] and Brachypodium distachyon [ 53 ] as monocot plants; and Fagopyrum tataricum [ 38 ], Solanum lycopersicum [ 32 , 37 , 54 ], Gossypium hirsutum [ 55 ], Camellia sinensis [ 56 ], Arabidopsis thaliana [ 22 , 24 , 36 , 43 , 57 , 58 ] and Brassica oleracea [ 23 ] as dicot plants. N -glycoproteomes have been described in different organs: whole thalli corresponding to the haploid gametophytic stage of M. polymorpha [ 52 ]; seedlings [ 59 ]; aerial organs for flowering plants, such as actively growing hypocotyls of etiolated seedlings [ 24 ]; leaves [ 33 , 34 , 43 , 56 ]; stems [ 22 , 43 ]; inflorescences [ 58 ]; fruit pericarp [ 32 , 37 , 54 ]; and seeds [ 38 , 55 ]. The N -glycoproteome of the xylem sap of B. oleracea has also been analyzed, and looks very similar to a cell wall proteome [ 23 ].…”

“…The study of N -glycoproteomes, thus, appears as a means to increase the coverage of cell wall proteomes ( Figure 5 ). To illustrate this point, three examples can be mentioned where the same plant material was used to prepare a cell wall proteome from purified cell walls and a N -glycoproteome: the thalli of M. polymorpha [ 52 ], the etiolated hypocotyls of A. thaliana [ 24 , 60 ], and the leaves of C. sinensis [ 56 ]. In the same way, the xylem sap proteome of B. oleracea was complemented with a N -glycoproteome [ 23 ].…”

Immunochemical Identification of the Main Cell Wall Polysaccharides of the Early Land Plant Marchantia polymorpha

“…The cell walls of mosses and liverworts were also found to contain p-coumaric and ferulic acids [18]. Regarding the cell wall proteins, we have recently provided a deep analysis of the cell wall proteome of M. polymorpha thalli and identified 410 different proteins, corresponding to about one third of the predicted cell wall proteome [27]. In addition, arabinogalactan proteins have been characterized in M. polymorpha and exhibit specific features, like the presence of terminal 3-O-methyl-rhamnose in their glycan moieties, and highly branched galactan side-chains that contain only traces of β-1,6-linked galactose, unlike angiosperms [28,29].…”