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Evolution of Cell Wall Polymers in Tip Evolution of Cell Wall Polymers in Tip-Growing Land Plant Gametophytes: Composition, Distribution, Functional Aspects and Their Remodeling Jérémy Dehors, Alain Mareck, Marie-Christine Kiefer-Meyer, Laurence Menu-Bouaouiche, Arnaud Lehner, Jean-Claude Mollet To cite this version: Jérémy Dehors, Alain Mareck, Marie-Christine Kiefer-Meyer, Laurence Menu-Bouaouiche, Arnaud Lehner, et al.. Evolution of Cell Wall Polymers in Tip-Growing Land Plant Gametophytes: Compo- sition, Distribution, Functional Aspects and Their Remodeling. Frontiers in Plant Science, Frontiers, 2019, 10, pp.441. 10.3389/fpls.2019.00441. hal-02115936 HAL Id: hal-02115936 https://hal-normandie-univ.archives-ouvertes.fr/hal-02115936 Submitted on 30 Apr 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEW published: 18 April 2019 doi: 10.3389/fpls.2019.00441 Evolution of Cell Wall Polymers in Tip-Growing Land Plant Gametophytes: Composition, Distribution, Functional Aspects and Their Remodeling Jérémy Dehors, Alain Mareck, Marie-Christine Kiefer-Meyer, Laurence Menu-Bouaouiche, Arnaud Lehner and Jean-Claude Mollet* Normandie Univ, UNIROUEN, Laboratoire de Glycobiologie et Matrice Extracellulaire Végétale, Rouen, France During evolution of land plants, the first colonizing species presented leafy-dominant gametophytes, found in non-vascular plants (bryophytes). Today, bryophytes include liverworts, mosses, and hornworts. In the first seedless vascular plants (lycophytes), the sporophytic stage of life started to be predominant. In the seed producing plants, Edited by: gymnosperms and angiosperms , the gametophytic stage is restricted to reproduction. In Zoë A. Popper, mosses and ferns, the haploid spores germinate and form a protonema, which develops National University of Ireland Galway, Ireland into a leafy gametophyte producing rhizoids for anchorage, water and nutrient uptakes. Reviewed by: The basal gymnosperms (cycads and Ginkgo) reproduce by zooidogamy. Their pollen Giampiero Cai, grains develop a multi-branched pollen tube that penetrates the nucellus and releases University of Siena, Italy Alison Roberts, flagellated sperm cells that swim to the egg cell. The pollen grain of other gymnosperms University of Rhode Island, (conifers and gnetophytes) as well as angiosperms germinates and produces a pollen United States tube that directly delivers the sperm cells to the ovule (siphonogamy). These different *Correspondence: gametophytes, which are short or long-lived structures, share a common tip-growing Jean-Claude Mollet [email protected] mode of cell expansion. Tip-growth requires a massive cell wall deposition to promote cell elongation, but also a tight spatial and temporal control of the cell wall remodeling Specialty section: in order to modulate the mechanical properties of the cell wall. The growth rate of This article was submitted to Plant Physiology, these cells is very variable depending on the structure and the species, ranging from a section of the journal very slow (protonemata, rhizoids, and some gymnosperm pollen tubes), to a slow Frontiers in Plant Science to fast-growth in other gymnosperms and angiosperms. In addition, the structural Received: 30 January 2019 diversity of the female counterparts in angiosperms (dry, semi-dry vs wet stigmas, Accepted: 22 March 2019 Published: 18 April 2019 short vs long, solid vs hollow styles) will impact the speed and efficiency of sperm Citation: delivery. As the evolution and diversity of the cell wall polysaccharides accompanied Dehors J, Mareck A, the diversification of cell wall structural proteins and remodeling enzymes, this review Kiefer-Meyer M-C, Menu-Bouaouiche L, Lehner A and focuses on our current knowledge on the biochemistry, the distribution and remodeling Mollet J-C (2019) Evolution of Cell of the main cell wall polymers (including cellulose, hemicelluloses, pectins, callose, Wall Polymers in Tip-Growing Land arabinogalactan-proteins and extensins), during the tip-expansion of gametophytes Plant Gametophytes: Composition, Distribution, Functional Aspects and from bryophytes, pteridophytes (lycophytes and monilophytes), gymnosperms and the Their Remodeling. monocot and eudicot angiosperms. Front. Plant Sci. 10:441. doi: 10.3389/fpls.2019.00441 Keywords: cell-wall, gametophyte, tip-growth, pollen-tube, protonema, rhizoid, evolution, land plants Frontiers in Plant Science | www.frontiersin.org 1 April 2019 | Volume 10 | Article 441 Dehors et al. Cell Wall Evolution in Tip-Growth 1. INTRODUCTION suggested by Bascom et al. (2018), these structures must possess some differences as they are either short-lived (pollen tubes) The early non-vascular plants that successfully colonized land or long-lived (protonemata, rhizoids) cells and they perform are thought to have been similar to extant bryophytes. Today, divergent functions. bryophytes include liverworts, mosses and hornworts. Later In contrast with rhizoids and protonemata, which must sense on, the seedless vascular plants appeared (lycophytes and external environmental signals, pollen tubes are specialized in monilophytes) (Figure 1). Bryophytes are characterized by a carrying the sperm cells to the ovules and must sense the female gametophyte stage of the life cycle. Then, during evolution, the environment cues allowing efficient guidance to the ovules and gametophyte life cycle was reduced gradually, and was restricted seed production (Higashiyama et al., 2003). To succeed in this solely to reproduction in seed plants (Niklas and Kutschera, 2010; process, the spatial and temporal controls of the pollen tube Lora et al., 2016; Hackenberg and Twell, 2019). To date, more growth are critical within the female tissues: stigma, style and than 90% of land plants are the sporophyte-dominant flowering ovary. These organs vary greatly depending on the species: plants (Williams and Mazer, 2016). stigmas can be wet, semi-dry or dry; styles can be short, long, The most studied seedless plant so far is the model moss solid or hollow, ovary can contain a wide range of ovule numbers Physcomitrella patens (Rensing et al., 2008). But recently, (Williams and Mazer, 2016). This will surely impact the duration attention has turned to other species, such as the liverwort and efficiency of reproduction. Marchantia polymorpha (Bowman et al., 2017), the lycophyte Another interesting difference between those tip-growing Selaginella moellendorffii (spike moss) (Figure 1) (Banks et al., cells is the growth rate. First, it has been shown in P. patens 2011) and the monilophyte Ceratopteris richardii (C-fern) that caulonemal cells expanded faster (≈ 20 µm/h) than (Banks, 1999; Leroux et al., 2013) (Figure 1), for which the chloronemal cells (≈ 6 µm/h) (Menand et al., 2007). Secondly, genome sequencing is under way. The genome sequencing an interesting survey presented by Williams et al. (2016) of other species having gametophyte tip-growth will allow revealed that pollen tubes from the gymnosperms cycads/Ginkgo comparative genomics for ortholog genes to those of model were the slowest growing cells with a growth rate between seed plants, such as the monocot crop Oryza sativa (rice) 1 and 5 µm/h. It is noteworthy that in these plants, pollen (International Rice Genome Sequencing Project, 2005) and tubes grow like a haustorium rather than tip-growing cells. the eudicot Arabidopsis thaliana (The Arabidopsis Genome In conifers/gnetophytes, pollen tubes represented a major Initiative, 2000). evolutionary step in the male gametophyte development of In the moss P. patens, gametophytic spores germinate and gymnosperms (Fernando, 2005) with a faster expanding pollen produce a multi-branched structure of filamentous protonemata. tube tip (1-15 µm/h) (Williams et al., 2016; Hackenberg and This structure consists of tip-growing chloronemal and Twell, 2019). Gametophytic protonemata from P patens and caulonemal cells that will produce leafy gametophores anchored rhizoids of mosses, liverworts and C-fern have growth rates to the soil by another tip-growing structure called rhizoid ranging between 5–20 µm/h and 10–400 µm/h, respectively (Menand et al., 2007). In addition to anchorage, rhizoids are (Williams et al., 2016). The fastest tip-growing cells are of main importance for water and nutrient absorptions (Jones angiosperms pollen tubes ranging from 10 to 20,000 µm/h with and Dolan, 2012). Atomic force microscopy and scanning an average growth rate between 500–1,000 µm/h for most of electron microscopy have revealed that long fibrillar structures, the 180 species studied (Williams, 2012; Williams et al., 2016). disorganized in the caulonemal apical cells, become oriented in Growth rate of pollen tubes has been obtained so far with in longitudinal arrays parallel to the growth axis in the proximal vitro experiments that consequently prevent the likely control of region (Wyatt et al., 2008) as it was observed in A. thaliana the tip-growth expansion by the female sporophyte (Lord, 2000). pollen tubes (Chebli et al., 2012). Menand et al. (2007) showed This wide difference of growth
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