Role and Evolution of the Extracellular Matrix in the Acquisition of Complex Multicellularity in Eukaryotes: A Macroalgal Perspective

Overview

Journal Genes (Basel)

Publisher MDPI

Date 2021 Aug 6

PMID 34356075

Citations 13

Authors

Bernard Kloareg

Yacine Badis

J Mark Cock

Gurvan Michel

Affiliations

Soon will be listed here.

Abstract

Multicellular eukaryotes are characterized by an expanded extracellular matrix (ECM) with a diversified composition. The ECM is involved in determining tissue texture, screening cells from the outside medium, development, and innate immunity, all of which are essential features in the biology of multicellular eukaryotes. This review addresses the origin and evolution of the ECM, with a focus on multicellular marine algae. We show that in these lineages the expansion of extracellular matrix played a major role in the acquisition of complex multicellularity through its capacity to connect, position, shield, and defend the cells. Multiple innovations were necessary during these evolutionary processes, leading to striking convergences in the structures and functions of the ECMs of algae, animals, and plants.

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References

Ulaganathan T, Helbert W, Kopel M, Banin E, Cygler M . Structure-function analyses of a PL24 family ulvan lyase reveal key features and suggest its catalytic mechanism. J Biol Chem. 2018; 293(11):4026-4036. PMC: 5857984. DOI: 10.1074/jbc.RA117.001642. View

Naretto A, Fanuel M, Ropartz D, Rogniaux H, Larocque R, Czjzek M . The agar-specific hydrolase AgaC from the marine bacterium defines a new GH16 protein subfamily. J Biol Chem. 2019; 294(17):6923-6939. PMC: 6497945. DOI: 10.1074/jbc.RA118.006609. View

Doblin M, Pettolino F, Wilson S, Campbell R, Burton R, Fincher G . A barley cellulose synthase-like CSLH gene mediates (1,3;1,4)-beta-D-glucan synthesis in transgenic Arabidopsis. Proc Natl Acad Sci U S A. 2009; 106(14):5996-6001. PMC: 2667043. DOI: 10.1073/pnas.0902019106. View

Rees D . Enzymic desulphation of porphyran. Biochem J. 1961; 80:449-53. PMC: 1243251. DOI: 10.1042/bj0800449. View

Nobles D, Romanovicz D, Brown Jr R . Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase?. Plant Physiol. 2001; 127(2):529-42. PMC: 125088. View

Shao Z, Zhang P, Lu C, Li S, Chen Z, Wang X . Transcriptome sequencing of Saccharina japonica sporophytes during whole developmental periods reveals regulatory networks underlying alginate and mannitol biosynthesis. BMC Genomics. 2019; 20(1):975. PMC: 6909449. DOI: 10.1186/s12864-019-6366-x. View

Michel G, Tonon T, Scornet D, Cock J, Kloareg B . Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol. 2010; 188(1):67-81. DOI: 10.1111/j.1469-8137.2010.03345.x. View

Kumar S, Stecher G, Li M, Knyaz C, Tamura K . MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-1549. PMC: 5967553. DOI: 10.1093/molbev/msy096. View

Yokoyama R . A Genomic Perspective on the Evolutionary Diversity of the Plant Cell Wall. Plants (Basel). 2020; 9(9). PMC: 7570368. DOI: 10.3390/plants9091195. View

10.

Dangl J, Horvath D, Staskawicz B . Pivoting the plant immune system from dissection to deployment. Science. 2013; 341(6147):746-51. PMC: 3869199. DOI: 10.1126/science.1236011. View

11.

Leblanc C, Colin C, Cosse A, Delage L, La Barre S, Morin P . Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie. 2006; 88(11):1773-85. DOI: 10.1016/j.biochi.2006.09.001. View

12.

Rui Y, Dinneny J . A wall with integrity: surveillance and maintenance of the plant cell wall under stress. New Phytol. 2019; 225(4):1428-1439. DOI: 10.1111/nph.16166. View

13.

Gow N, Latge J, Munro C . The Fungal Cell Wall: Structure, Biosynthesis, and Function. Microbiol Spectr. 2017; 5(3). PMC: 11687499. DOI: 10.1128/microbiolspec.FUNK-0035-2016. View

14.

Sakai T, Ishizuka K, Shimanaka K, Ikai K, Kato I . Structures of oligosaccharides derived from Cladosiphon okamuranus fucoidan by digestion with marine bacterial enzymes. Mar Biotechnol (NY). 2004; 5(6):536-44. DOI: 10.1007/s10126-002-0107-9. View

15.

Urbach J, Ausubel F . The NBS-LRR architectures of plant R-proteins and metazoan NLRs evolved in independent events. Proc Natl Acad Sci U S A. 2017; 114(5):1063-1068. PMC: 5293065. DOI: 10.1073/pnas.1619730114. View

16.

Dhugga K, Barreiro R, Whitten B, Stecca K, Hazebroek J, Randhawa G . Guar seed beta-mannan synthase is a member of the cellulose synthase super gene family. Science. 2004; 303(5656):363-6. DOI: 10.1126/science.1090908. View

17.

Rees D . Structure, conformation, and mechanism in the formation of polysaccharide gels and networks. Adv Carbohydr Chem Biochem. 1969; 24:267-332. DOI: 10.1016/s0065-2318(08)60352-2. View

18.

Maekawa T, Kufer T, Schulze-Lefert P . NLR functions in plant and animal immune systems: so far and yet so close. Nat Immunol. 2011; 12(9):817-26. DOI: 10.1038/ni.2083. View

19.

Collen J, Porcel B, Carre W, Ball S, Chaparro C, Tonon T . Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A. 2013; 110(13):5247-52. PMC: 3612618. DOI: 10.1073/pnas.1221259110. View

20.

Yin Y, Huang J, Xu Y . The cellulose synthase superfamily in fully sequenced plants and algae. BMC Plant Biol. 2009; 9:99. PMC: 3091534. DOI: 10.1186/1471-2229-9-99. View