Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants

Popper, Zoë A.; Michel, Gurvan; Hervé, Cécile; Domozych, David S.; Willats, William G.T.; Tuohy, Maria G.; Kloareg, Bernard; Stengel, Dagmar B.

doi:10.1146/annurev-arplant-042110-103809

Cited by 620 publications

(500 citation statements)

References 138 publications

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“…Cellulose synthase (CesA) and cellulose synthase-like (Csl) genes are considered to play a role in influencing the biomechanical properties of the cell 35 , hence potentially the distinctive growth forms of gnetophytes are associated with the divergence of these genes. To explore this hypothesis, CesA and Csl family members were examined in G. montanum and compared with those in other seed plants.…”

Section: Growth Form (Shrubs and Lianas) And Leaf Morphologymentioning

confidence: 99%

A genome for gnetophytes and early evolution of seed plants

et al. 2018

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Gnetophytes are an enigmatic gymnosperm lineage comprising three genera, Gnetum, Welwitschia and Ephedra, which are morphologically distinct from all other seed plants. Their distinctiveness has triggered much debate as to their origin, evolution and phylogenetic placement among seed plants. To increase our understanding of the evolution of gnetophytes, and their relation to other seed plants, we report here a high-quality draft genome sequence for Gnetum montanum, the first for any gnetophyte. By using a novel genome assembly strategy to deal with high levels of heterozygosity, we assembled >4 Gb of sequence encoding 27,491 protein-coding genes. Comparative analysis of the G. montanum genome with other gymnosperm genomes unveiled some remarkable and distinctive genomic features, such as a diverse assemblage of retrotransposons with evidence for elevated frequencies of elimination rather than accumulation, considerable differences in intron architecture, including both length distribution and proportions of (retro) transposon elements, and distinctive patterns of proliferation of functional protein domains. Furthermore, a few gene families showed Gnetum-specific copy number expansions (for example, cellulose synthase) or contractions (for example, Late Embryogenesis Abundant protein), which could be connected with Gnetum's distinctive morphological innovations associated with their adaptation to warm, mesic environments. Overall, the G. montanum genome enables a better resolution of ancestral genomic features within seed plants, and the identification of genomic characters that distinguish Gnetum from other gymnosperms. NATuRe PLANTS ArticlesNATurE PLANTs phylogenetic position of gnetophytes, with topologies differing depending on the type of sequence data (for example, plastid versus nuclear genes, nucleotide versus amino acid data) and analytical approach used (for example, maximum parsimony, maximum likelihood, Bayesian, multispecies coalescent based methods) [6][7][8] . Consequently, several possible hypotheses have been put forward that place gnetophytes as sister to (1) Pinaceae ('Gnepine' hypothesis); (2) cupressophytes ('Gnecup' hypothesis); (3) all conifers ('Gnetifer' hypothesis); (4) all other gymnosperms; or (5) all seed plants 9 . Currently, the emerging consensus, based on both older and more recent studies, and recently released data from the 1KP initiative (see https://sites.google.com/a/ualberta.ca/onekp/, and Wickett et al. 8 ), indicates that gnetophytes are sister to, or within, the conifers.So far, the availability of whole genome sequences for gymnosperms has been limited to conifers (specifically to Pinaceae) [10][11][12][13] and G. biloba 14 , with no whole genome assemblies available for the two remaining major seed plant lineages-cycads and gnetophytes. This deficiency, together with the conflicting phylogenetic evidence for relationships among these groups, is impeding our understanding of genome evolution across all seed plants. Here, we present a high-quality draft genome of Gnetum ...

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Section: Growth Form (Shrubs and Lianas) And Leaf Morphologymentioning

confidence: 99%

A genome for gnetophytes and early evolution of seed plants

et al. 2018

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“…Some species have no cell wall, whereas walled species use a variety of wall polymers including cellulose, pectins, chitin-like molecules, or hydroxyproline-rich glycoproteins. Besides sugar-polymer-based walls, some species cover themselves with hard calcified scales (Popper et al 2011;Domozych et al 2012;Leliaert et al 2012).…”

Section: Multicellularity In Green Algae and Plantsmentioning

confidence: 99%

“…Cellulosic walls are found throughout the green algal lineage and in other taxa, but a hexameric cellulose synthase complex evolved uniquely in streptophytes (Tsekos 1999). Other distinctive characteristics of embryophyte cell walls, including complex carbohydrate polymer linkages, first appeared in advanced charophyte green algae (Van Sandt et al 2007;Popper et al 2011;Sørensen et al 2011;Domozych et al 2012;Proseus and Boyer 2012). The recent discovery of expansin genes in the Zygnematophycean alga Micrasterias suggests that these critical cell wall remodeling proteins from embryophytes originated in charophyte algae (Cosgrove 2000;Vannerum et al 2011).…”

Section: Multicellular Innovations In Land Plants That May Be Rooted mentioning

confidence: 99%

Green Algae and the Origins of Multicellularity in the Plant Kingdom

Umen

2014

Cold Spring Harbor Perspectives in Biology

121

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The green lineage of chlorophyte algae and streptophytes form a large and diverse clade with multiple independent transitions to produce multicellular and/or macroscopically complex organization. In this review, I focus on two of the best-studied multicellular groups of green algae: charophytes and volvocines. Charophyte algae are the closest relatives of land plants and encompass the transition from unicellularity to simple multicellularity. Many of the innovations present in land plants have their roots in the cell and developmental biology of charophyte algae. Volvocine algae evolved an independent route to multicellularity that is captured by a graded series of increasing cell-type specialization and developmental complexity. The study of volvocine algae has provided unprecedented insights into the innovations required to achieve multicellularity.

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“…Synthesis of cutin-cuticular waxes to the outside of the leaf epidermis and suberin-lignin near the plasma membrane (Supplementary Note 9, Supplementary Table 9.1) surround a cell wall matrix of (hemi)celluloses, low-methylated pectin (zosterin) and macroalgal-like sulfated polysaccharides 18 (Supplementary Note 10). The reduction in carbohydrate-related genes that modify the fine structure of cell wall hemicelluloses and pectins in Z. marina is not due to loss of pathways, but rather to the large variation within these CAZyme gene families in plants.…”

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confidence: 99%

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

Olsen

Rouzé

Verhelst

et al. 2016

Nature

Self Cite

458

486

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Seagrasses colonized the sea 1 on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet 2 . Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes 3 , genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae 4 and that is important for ion homoeostasis, nutrient uptake and O 2 /CO 2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming 5,6 , to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants 7

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Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants

Cited by 620 publications

References 138 publications

A genome for gnetophytes and early evolution of seed plants

A genome for gnetophytes and early evolution of seed plants

Green Algae and the Origins of Multicellularity in the Plant Kingdom

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

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