Evolution of Cell Wall Polymers in Tip-Growing Land Plant Gametophytes: Composition, Distribution, Functional Aspects and Their Remodeling

Dehors, Jérémy; Mareck, Alain; Kiefer‐Meyer, Marie‐Christine; Menu-Bouaouiche, Laurence; Lehner, Arnaud; Mollet, Jean‐Claude

doi:10.3389/fpls.2019.00441

Cited by 44 publications

(46 citation statements)

References 297 publications

(544 reference statements)

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“…In fact, in pollen tubes the fine control of modulation of the DM is of major importance during growth (Wolf et al, 2009). As previously described in Arabidopsis as well as in many other species such as potato, tobacco, petunia, jasmine, maize and lily (Dardelle et al, 2010;Chebli et al, 2012;Mollet et al, 2013;Dehors et al, 2019), immunolabeling showed that in Amaryllis, the pollen used for this study, highly methylesterified HGs are dominantly localized in the apical region and weakly methylesterified HGs prevail in the subapical region and the shank of the pollen tube. Modulation of the DM is thought to provide sufficient plasticity in the apical cell wall to sustain pollen tube growth (Chebli and Geitmann, 2007), whereas in the subapical region methylesterified HGs are processed by PMEs.…”

Section: Discussionsupporting

confidence: 71%

The exogenous application of AtPGLR, an endo‐polygalacturonase, triggers pollen tube burst and repair

et al. 2020

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SUMMARY Plant cell wall remodeling plays a key role in the control of cell elongation and differentiation. In particular, fine‐tuning of the degree of methylesterification of pectins was previously reported to control developmental processes as diverse as pollen germination, pollen tube elongation, emergence of primordia or elongation of dark‐grown hypocotyls. However, how pectin degradation can modulate plant development has remained elusive. Here we report the characterization of a polygalacturonase (PG), AtPGLR, the gene for which is highly expressed at the onset of lateral root emergence in Arabidopsis. Due to gene compensation mechanisms, mutant approaches failed to determine the involvement of AtPGLR in plant growth. To overcome this issue, AtPGLR has been expressed heterologously in the yeast Pichia pastoris and biochemically characterized. We showed that AtPGLR is an endo‐PG that preferentially releases non‐methylesterified oligogalacturonides with a short degree of polymerization (< 8) at acidic pH. The application of the purified recombinant protein on Amaryllis pollen tubes, an excellent model for studying cell wall remodeling at acidic pH, induced abnormal pollen tubes or cytoplasmic leakage in the subapical dome of the pollen tube tip, where non‐methylesterified pectin epitopes are detected. Those leaks could either be repaired by new β‐glucan deposits (mostly callose) in the cell wall or promoted dramatic burst of the pollen tube. Our work presents the full biochemical characterization of an Arabidopsis PG and highlights the importance of pectin integrity in pollen tube elongation.

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Section: Discussionsupporting

confidence: 71%

The exogenous application of AtPGLR, an endo‐polygalacturonase, triggers pollen tube burst and repair

et al. 2020

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“…The colonization of terrestrial habitats by embryophytes has been dependent upon the ability to synthesize complex cell walls that provide biomechanical support and protection against environmental stresses. Land plant primary walls are comprised of a core scaffolding of cellulose microfibrils embedded within matrices of interconnecting pectin and hemicellulose polysaccharides, together with glycoproteins (Burton et al, 2010; Popper et al, 2011; Dehors et al, 2019). However, immunological and biochemical studies suggest that the capacity to synthesize many of the polysaccharides of extant embryophyte walls evolved prior to the ancestral land plant, during divergence of the charophyte algae (Sørensen et al, 2011).…”

Section: Resultsmentioning

confidence: 99%

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

Jiao

Sørensen

Sun

et al. 2019

Preprint

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30The colonization of land by plants was a pivotal event in the history of the biosphere, and yet the 31 underlying evolutionary features and innovations of the first land plant ancestors are not well 32 understood. Here we present the genome sequence of the unicellular alga Penium margaritaceum, 33 a member of the Zygnematophyceae, the sister lineage to land plants. The P. margaritaceum 34 genome has a high proportion of repeat sequences, which are associated with massive segmental 35 gene duplications, likely facilitating neofunctionalization. Compared with earlier diverging plant 36 lineages, P. margaritaceum has uniquely expanded repertoires of gene families, signaling 37 networks and adaptive responses, supporting its phylogenetic placement and highlighting the 38 evolutionary trajectory towards terrestrialization. These encompass a broad range of physiological 39 processes and cellular structures, such as large families of extracellular polymer biosynthetic and 40 modifying enzymes involved in cell wall assembly and remodeling. Transcriptome profiling of 41 cells exposed to conditions that are common in terrestrial habitats, namely high light and 42 desiccation, further elucidated key adaptations to the semi-aquatic ecosystems that are home to the 43 Zygnematophyceae. Such habitats, in which a simpler body plan would be advantageous, likely 44 provided the evolutionary crucible in which selective pressures shaped the transition to land. 45 Earlier diverging charophyte lineages that are characterized by more complex land plant-like 46 anatomies have either remained exclusively aquatic, or developed alternative life styles that allow 47 109 of 116.1 kb. The nuclear assembly captured most of the k-mers in the Illumina reads and low 110 frequency k-mers representing sequencing errors were absent ( Supplementary Fig. 1B). In addition, 111 the mapping rates of genomic and RNA-Seq reads against the nuclear assembly were 97.5% and 112 5 96.8%, respectively (Supplementary Table 2). The single nucleotide polymorphism (SNP) 113 frequency distribution on the 100 longest scaffolds was consistent with a haploid genome 114 ( Supplementary Fig. 1C). The mitochondrial and chloroplast genomes were also fully assembled, 115 and comprised 95,332 and 145,411 nucleotides, respectively ( Supplementary Fig. 2). 116The assembly contains a large proportion (80.6%) of repeat sequences (Supplementary 117 Table 3), particularly long terminal repeat (LTR) retrotransposons and simple repeats ( Fig. 2A). 118Unlike land plants and C. braunii, in which gypsy is the predominant LTR family, the P. 119 margaritaceum genome has a large proportion of copia retrotransposons, which are rare in other 120 green algae and absent from C. braunii (Nishiyama et al. 2018). An estimation of divergence time 121 indicated that the copia expansion in the P. margaritaceum genome was relatively recent, around 122 2.1 Mya (Fig. 2B). Retrotransposons carrying tyrosine recombinases, such as the DIRS and Ngaro 123 families, which are found in some chlorophyte...

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“…Furthermore, higher order RK mutant pistils show differences in the morphology of callose plugs within the wild-type Col-0 pollen tubes (Figure 3K-3L). Callose plugs are deposited to separate the growing pollen tube tip from the older part of the tube, and they are typically elongated in shape at 2-hours post-pollinations [42, 43] as seen for the Col-0 pollen tubes growing in Col-0 pistils and some of the RK mutant pistils (Figure 3A-3C, 3E and 3J). However, in some of the higher order mutants, the callose plugs were not elongated (Figure 3D, 3F-3H, 3K and 3L).…”

Section: Resultsmentioning

confidence: 99%

“…Finally, smaller callose plugs were observed in the wild-type pollen tubes growing through the higher order RK mutant pistils. Pollen tubes sustain rapid polarized growth by depositing callose plugs to maintain turgor pressure and concentrate the cytoplasmic content at the growing tip [43, 46]. The loss of the signaling dialog between the pollen tube and these RKs in the stigma/style transmitting tissue may cause the wild-type pollen tube to have reduced access to components needed for proper callose plug formation.…”

Section: Discussionmentioning

confidence: 99%

Two groups of Arabidopsis receptor kinases preferentially regulate the growth of intraspecies pollen tubes in the female reproductive tract

Lee

Goring

2020

Preprint

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In flowering plants, continuous cell-cell communication between the compatible male pollen 15 grain/growing pollen tube and the female pistil is required for successful sexual reproduction. In 16Arabidopsis thaliana, the later stages of this dialogue are mediated by several peptide ligands 17 and receptor kinases that guide pollen tubes to the ovules for the release of sperm cells. Despite a 18 detailed understanding of these processes, a key gap remains on the nature of the regulators that 19 function at the earlier stages. Here, we report on two groups of A. thaliana receptor kinases, the 20 LRR-VIII-2 RK subclass and the SERKs, that function in the female reproductive tract to regulate 21 the compatible pollen grains and early pollen tube growth, both essential steps for the 22 downstream processes leading to fertilization. Multiple A. thaliana LRR-VIII-2 RK and SERK 23 knockout mutant combinations were created, and several phenotypes were observed such as 24 reduced wild-type pollen hydration and reduced pollen tube travel distances. As these mutant 25 pistils displayed a wild-type morphology, the observed altered responses of the wild-type pollen 26 are proposed to result from the loss of these receptor kinases leading to an impaired pollen-pistil 27 dialogue at these early stages. Furthermore, using pollen from related Brassicaceae species, we 28 also discovered that these receptor kinases are required in the female reproductive tract to 29 establish a reproductive barrier to interspecies pollen. Thus, we propose that the LRR-VIII-2 RKs 30 and the SERKs play a dual role in the preferential selection and promotion of intraspecies pollen 31 over interspecies pollen. 32 33 Key Words: Arabidopsis, receptor kinases, pollen, pistil, compatible intraspecies pollinations, 34 interspecies pollinations 35 is the identification of the key regulators that function in the earlier stages that take place in the 63 stigma/style immediately after pollination. Successful growth of pollen tubes through the A. 64 thaliana stigma/style is a prerequisite to these later stages as pollen tubes growing through the 65 stigma/style then acquire the competency to perceive ovular guidance cues [23]. So far, the only 66 4 putative early stage regulators that have been identified are the pollen-specific genes encoding 67 the Pollen Coat Protein-B (PCP-B) peptides which are required for pollen adhesion and 68 hydration [24]. 69Here, we report that members of two groups of RK genes, the LEUCINE RICH REPEAT (LRR)-70 VIII-2 RKs and the SOMATIC EMBRYOGENESIS RECEPTOR KINASES (SERKs), that are 71 required in the stigma and the female reproductive tract to promote compatible pollen grain 72 hydration and pollen tube growth and to establish a reproductive barrier against interspecies 73 pollen tube growth. The discovery of these RKs was enabled by employing an unconventional 74 approach of using an interspecies tissue-specific pseudokinase as a tool for discovery of 75 candidate RKs by using the assumption that pseudokinases typically associate ...

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Evolution of Cell Wall Polymers in Tip-Growing Land Plant Gametophytes: Composition, Distribution, Functional Aspects and Their Remodeling

Cited by 44 publications

References 297 publications

The exogenous application of AtPGLR, an endo‐polygalacturonase, triggers pollen tube burst and repair

The exogenous application of AtPGLR, an endo‐polygalacturonase, triggers pollen tube burst and repair

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

Two groups of Arabidopsis receptor kinases preferentially regulate the growth of intraspecies pollen tubes in the female reproductive tract

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