A phenol-enriched cuticle is ancestral to lignin evolution in land plants

Renault, H; Alber, A.; Horst, Nelly A.; Lopes, Alexandra Basilio; Fich, Eric A.; Kriegshauser, Lucie; Wiedemann, Gertrud; Ullmann, Pascaline; Herrgott, Laurence; Erhardt, Mathieu; Pineau, Emmanuelle; Ehlting, Jürgen; Schmitt, Martine; Rose, Jocelyn K. C.; Reski, Ralf; Werck‐Reichhart, Danièle

doi:10.1038/ncomms14713

Cited by 173 publications

(169 citation statements)

References 39 publications

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“…The single CYP98 of P. patens was recently found to have activity with a 4‐coumaric ester of threonic acid. It is essential for the accumulation of soluble caffeoyl‐threonate and for the formation of a phenolic monomer‐enriched cuticle polymer (Renault et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Evolution of coumaroyl conjugate 3‐hydroxylases in land plants: lignin biosynthesis and defense

et al. 2019

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Summary Multiple adaptations were necessary when plants conquered the land. Among them were soluble phenylpropanoids related to plant protection and lignin necessary for upright growth and long‐distance water transport. Cytochrome P450 monooxygenase 98 (CYP98) catalyzes a rate‐limiting step in phenylpropanoid biosynthesis. Phylogenetic reconstructions suggest that a single copy of CYP98 founded each major land plant lineage (bryophytes, lycophytes, monilophytes, gymnosperms and angiosperms), and was maintained as a single copy in all lineages but the angiosperms. In angiosperms, a series of independent gene duplications and losses occurred. Biochemical assays in four angiosperm species tested showed that 4‐coumaroyl‐shikimate, a known intermediate in lignin biosynthesis, was the preferred substrate of one member in each species, while independent duplicates in Populus trichocarpa and Amborella trichopoda each showed broad substrate ranges, accepting numerous 4‐coumaroyl‐esters and ‐amines, and were thus capable of producing a wide range of hydroxycinnamoyl conjugates. The gymnosperm CYP98 from Pinus taeda showed a broad substrate range, but preferred 4‐coumaroyl‐shikimate as its best substrate. In contrast, CYP98s from the lycophyte Selaginella moellendorffii and the fern Pteris vittata converted 4‐coumaroyl‐shikimate poorly in vitro, but were able to use alternative substrates, in particular 4‐coumaroyl‐anthranilate. Thus, caffeoyl‐shikimate appears unlikely to be an intermediate in monolignol biosynthesis in non‐seed vascular plants, including ferns. The best substrate for CYP98A34 from the moss Physcomitrella patens was also 4‐coumaroyl‐anthranilate, while 4‐coumaroyl‐shikimate was converted to lower extents. Despite having in vitro activity with 4‐coumaroyl‐shikimate, CYP98A34 was unable to complement the Arabidopsis thaliana cyp98a3 loss‐of‐function phenotype, suggesting distinct properties also in vivo.

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Section: Introductionmentioning

confidence: 97%

Evolution of coumaroyl conjugate 3‐hydroxylases in land plants: lignin biosynthesis and defense

et al. 2019

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“…Anyway, with systematic approaches it will definitely be possible to significantly advance our knowledge in a few years from now. Mosses and liverworts are emerging as models for studies on the assembly, function and evolution of the plant cuticle (31,85,86 …”

Section: Structural Plasticity Of Ltpsmentioning

confidence: 99%

Plant lipid transfer proteins: are we finally closing in on the roles of these enigmatic proteins?

Edqvist

Blomqvist

Nieuwland

et al. 2018

Journal of Lipid Research

100

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The nonspecific lipid transfer proteins (LTPs) are small, compact proteins folded around a tunnel-like hydrophobic cavity, making them suitable for lipid binding and transport. LTPs are encoded by large gene families in all land plants, but they have not been identified in algae or any other organisms. Thus, LTPs are considered key proteins for plant survival on and colonization of land. LTPs are abundantly expressed in most plant tissues, both above and below ground. They are usually localized to extracellular spaces outside the plasma membrane. Although the in vivo functions of LTPs remain unclear, accumulating evidence suggests a role for LTPs in the transfer and deposition of monomers required for assembly of the water-proof lipid barriers-such as cutin and cuticular wax, suberin, and sporopolleninformed on many plant surfaces. Some LTPs may be involved in other processes, such as signaling during pathogen attacks. Here, we present the current status of LTP research with a focus on the role of these proteins in lipid barrier deposition and cell expansion. We suggest that LTPs facilitate extracellular transfer of barrier materials and adhesion between barriers and extracellular materials. A growing body of research may uncover the true role of LTPs in plants. Overview of plant non-specific lipid transfer proteinsThe plant non-specific lipid transfer proteins (LTPs) are abundant, secreted, soluble, cysteinerich and small proteins with a molecular size usually below 10 kDa (1, 2). In the LTPs four conserved disulfide bridges, formed by an eight-Cys motif (8CM) with the general form CXn-C-Xn-CC-Xn-CXC-Xn-C-Xn-C, stabilize the folding of four or five α-helices into a very compact 3D-structure (3, 4 and Fig. 1). The folding of the helices results in a central hydrophobic cleft suitable for the binding of hydrophobic ligands, such as fatty acids and other lipids (Fig. 2). The compact structure renders the LTPs very insensitive to heat and denaturing agents (5, 6). LTPs are expressed in all investigated land plants, but have not been detected in any other organisms (7). LTPs are encoded by large gene families in seed plants (2,(8)(9)(10)(11). In bryophytes and ferns the gene families are significantly smaller (7,12). LTPs are classified in five major types (LTP1, LTP2, LTPc, LTPd and LTPg) and four minor types (LTPe, LTPf, LTPh, LTPj and LTPk) (7). The classification is based on the spacing between the Cys residues in the 8CM, the polypeptide sequence identity and the position of evolutionary conserved introns. The classification also reflects post-translational modifications, e.g. LTPs with a GPI-anchor belong to LTPg. LTPd and LTPg are encoded in all land plants which suggests that these were possibly the first LTP types that evolved in land plants. The most well-studied LTP types in flowering plants LTP1 and LTP2 probably evolved later since these are not found in liverworts, mosses or other non-seed plants (7). The LTPs are translated with an N-terminal signal peptide that has a potential to localize th...

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“…If so, a UV‐dependent ecological segregation of liverworts and mosses could have happened in these earliest diverging land plants (Bowman et al., ; Qiu et al., ; Wickett et al., ) upon land colonization. This would support the importance of UV radiation as an evolutionary factor and the relevance of cell wall‐bound phenolic compounds to improve UV adaptation during plant terrestrialization (Graham et al., ; Harholt et al., ; Ligrone et al., ; Lowry et al., ; Renault et al., ; Wallace et al., ). Thus, bryophyte UVACs compartmentation is revealed as an underexplored tool which could be tested in different phylogenetic groups of photosynthetic organisms to better understand their adaptation to a new UV regime in the water‐to‐land transition.…”

Section: Discussionmentioning

confidence: 75%

Cell compartmentation of ultraviolet‐absorbing compounds: An underexplored tool related to bryophyte ecology, phylogeny and evolution

2018

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Excessive exposure to ultraviolet (UV) radiation can be harmful to photosynthetic organisms, that most frequently respond with the accumulation of protective UV‐absorbing compounds (UVACs). UVACs location in different cell compartments can influence their preferential protective role as antioxidants and/or UV screens. However, the phylogenetic, ecological and evolutionary implications of UVACs compartmentation has been little studied, particularly in bryophytes. We analysed UVACs in the methanol‐soluble and ‐insoluble fractions (SUVACs and IUVACs respectively) in extracts of 87 bryophytes belonging to their three evolutionary lineages: 22 liverworts, 64 mosses and one hornwort. Assuming that the cell wall‐bound IUVACs are more effective UV screens than the mainly vacuolar SUVACs, thus conferring a higher UV tolerance, we evaluated whether UVACs levels and compartmentation were related to: (1) the bryophyte phylogeny down to the Order level; and (2) the bryophyte ecological attributes, including sun exposure and Ellenberg indicator values (numerical system classifying species' habitat along gradients of environmental factors). A similar phylogenetic and ecological analysis was conducted on the sclerophylly index (the ratio between the dry mass and the surface area of the bryophyte shoot). Mosses showed lower SUVACs but higher IUVACs and total UVACs, together with higher IUVAC/SUVAC ratios, than liverworts. Thus, mosses would better tolerate UV radiation than liverworts, which matches well with their general ecological preferences. As bryophytes were the earliest diverging land plants, we could infer that the different UVACs compartmentation between mosses and liverworts could have influenced their ecological segregation upon plant land colonization. UVACs compartmentation also differed between the two major moss lineages (acrocarpous and pleurocarpous), while the anatomically peculiar Sphagnales were the best characterized Order. There were not solid relationships between UVACs and the ecological attributes considered. Hence, UVACs might be mainly constitutive in bryophytes, depending more on the species phylogeny than on the habitat occupied in nature. Liverworts were less sclerophyllous than mosses, and, as in tracheophytes, water restrictions and high sun exposures increased sclerophylly. In conclusion, UVACs compartmentation represents an ecophysiological trait useful to understand the bryophyte ecophylogeny, because different compartmentation modalities seem to imply different UV adaptations and tolerance. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13048/suppinfo is available for this article.

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A phenol-enriched cuticle is ancestral to lignin evolution in land plants

Cited by 173 publications

References 39 publications

Evolution of coumaroyl conjugate 3‐hydroxylases in land plants: lignin biosynthesis and defense

Evolution of coumaroyl conjugate 3‐hydroxylases in land plants: lignin biosynthesis and defense

Plant lipid transfer proteins: are we finally closing in on the roles of these enigmatic proteins?

Cell compartmentation of ultraviolet‐absorbing compounds: An underexplored tool related to bryophyte ecology, phylogeny and evolution

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