Arabinogalactan proteins: Distribution during the development of male and female gametophytes

Leszczuk, Agata; Szczuka, Ewa; Zdunek, Artur

doi:10.1016/j.plaphy.2018.11.023

Cited by 29 publications

(28 citation statements)

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“…Other possible roles for AGPs and/or the glycan chains on AGPs were investigated by immunolocalization in numerous plant species [44] and could be an area of future research. The development of AGP monoclonal antibodies (e.g.…”

Section: Agp Glycosylation Functions In Both Male and Female Gametophmentioning

confidence: 99%

CRISPR-Cas9 multiplex genome editing of the hydroxyproline-O-galactosyltransferase gene family alters arabinogalactan-protein glycosylation and function in Arabidopsis

et al. 2021

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Background Arabinogalactan-proteins (AGPs) are a class of hydroxyproline-rich proteins (HRGPs) that are heavily glycosylated (> 90%) with type II arabinogalactans (AGs). AGPs are implicated in various plant growth and development processes including cell expansion, somatic embryogenesis, root and stem growth, salt tolerance, hormone signaling, male and female gametophyte development, and defense. To date, eight Hyp-O-galactosyltransferases (GALT2–6, HPGT1–3) have been identified; these enzymes are responsible for adding the first sugar, galactose, onto AGPs. Due to gene redundancy among the GALTs, single or double galt genetic knockout mutants are often not sufficient to fully reveal their biological functions. Results Here, we report the successful application of CRISPR-Cas9 gene editing/multiplexing technology to generate higher-order knockout mutants of five members of the GALT gene family (GALT2–6). AGPs analysis of higher-order galt mutants (galt2 galt5, galt3 galt4 galt6, and galt2 galt3 galt4 galt5 gal6) demonstrated significantly less glycosylated AGPs in rosette leaves, stems, and siliques compared to the corresponding wild-type organs. Monosaccharide composition analysis of AGPs isolated from rosette leaves revealed significant decreases in arabinose and galactose in all the higher-order galt mutants. Phenotypic analyses revealed that mutation of two or more GALT genes was able to overcome the growth inhibitory effect of β-D-Gal-Yariv reagent, which specifically binds to β-1,3-galactan backbones on AGPs. In addition, the galt2 galt3 galt4 galt5 gal6 mutant exhibited reduced overall growth, impaired root growth, abnormal pollen, shorter siliques, and reduced seed set. Reciprocal crossing experiments demonstrated that galt2 galt3 galt4 galt5 gal6 mutants had defects in the female gametophyte which were responsible for reduced seed set. Conclusions Our CRISPR/Cas9 gene editing/multiplexing approach provides a simpler and faster way to generate higher-order mutants for functional characterization compared to conventional genetic crossing of T-DNA mutant lines. Higher-order galt mutants produced and characterized in this study provide insight into the relationship between sugar decorations and the various biological functions attributed to AGPs in plants.

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Section: Agp Glycosylation Functions In Both Male and Female Gametophmentioning

confidence: 99%

CRISPR-Cas9 multiplex genome editing of the hydroxyproline-O-galactosyltransferase gene family alters arabinogalactan-protein glycosylation and function in Arabidopsis

et al. 2021

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“…The presence of AGPs within pollen tubes has been documented in diverse plant species, mainly at their apex [ 27 , 52 , 53 ]. A specific subset of AGPs was shown to be not only important for pollen development but also good candidates to mediate pollen tube growth.…”

Section: Discussionmentioning

confidence: 99%

“…The plasma membrane and Hechtian strand localization of FLA14 was implied to mediate its function in cell adhesion and signaling during pollen germination [ 36 ]. It has been hypothesized that external dynamic storage by a periplasmic AGP flux capacitor may be associated with the adaptation of the cell to changing conditions and its response to stress factors [ 27 , 66 , 67 ]. Based on this hypothesis, we speculate that interference of the plasma membrane and Hechtian strand-localized FLA14 might disturb the sensing of external signals and disrupt periplasmic AGP-Ca 2+ dissociation, as well as destabilize networks in pollen grains and pollen tubes, causing failure in the pollen tube response to high humidity and prevention of premature pollen germination inside the anthers.…”

Section: Discussionmentioning

confidence: 99%

“…To date, a total of 85 and 282 putative AGPs have been identified in the Arabidopsis genome and the Oryza sativa genome, respectively [ 16 , 17 ]. Previous studies have demonstrated that AGPs are extensively implicated in diverse plant growth and development processes under different conditions, such as sexual reproduction (microspore development, female gametogenesis, embryo development, pollen-pistil interaction, pollen germination, and pollen tube growth), vegetative growth (stem development, vascular tissue function, and root development), programmed cell death, cell division and expansion, and response to abiotic stress [ 13 , 15 , 18 – 27 ].…”

Section: Introductionmentioning

confidence: 99%

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FLA14 is required for pollen development and preventing premature pollen germination under high humidity in Arabidopsis

et al. 2021

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Background As an important subfamily of arabinogalactan proteins (AGPs), fasciclin-like AGPs (FLAs) contribute to various aspects of growth, development and adaptation, yet their function remains largely elusive. Despite the diversity of FLAs, only two members, Arabidopsis FLA3 and rice MTR1, are reported to be involved in sexual reproduction. In this study, another Arabidopsis FLA-encoding gene, FLA14, was identified, and its role was investigated. Results Arabidopsis FLA14 was found to be a pollen grain-specific gene. Expression results from fusion with green fluorescent protein showed that FLA14 was localized along the cell membrane and in Hechtian strands. A loss-of-function mutant of FLA14 showed no discernible defects during male gametogenesis, but precocious pollen germination occurred inside the mature anthers under high moisture conditions. Overexpression of FLA14 caused 39.2% abnormal pollen grains with a shrunken and withered appearance, leading to largely reduced fertility with short mature siliques and lower seed set. Cytological and ultramicroscopic observation showed that ectopic expression of FLA14 caused disruption at the uninucleate stage, resulting in either collapsed pollen with absent intine or pollen of normal appearance but with a thickened intine. Conclusions Taken together, our data suggest a role for FLA14 in pollen development and preventing premature pollen germination inside the anthers under high relative humidity in Arabidopsis.

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“…In seed plants, the extracellular matrix (ecm) of the female reproductive organs is the site of interactions with the male gametophyte, which begins during pollination and continues throughout the progamic phase. Many studies of model angiosperm plants have revealed the important role of pectins (HomoGalacturonans, HGs) and ArabinoGalactan Proteins (AGPs) in these processes [1][2][3][4]. The interaction results in a change in the activity of the wall enzymes of both reproductive partners, leading to alterations in the composition of the extracellular matrix (ecm), including the level of Ca 2+ ions relevant for germination, pollen tube growth and double fertilization [5][6][7].…”

Section: Introductionmentioning

confidence: 99%

Spatial and Temporal Distribution of Arabinogalactan Proteins during Larix decidua Mill. Male Gametophyte and Ovule Interaction

Rafińska

Niedojadło

Świdziński

et al. 2021

IJMS

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The role of ArabinoGalactan Proteins (AGPs) in the sexual reproduction of gymnosperms is not as well documented as that of angiosperms. In earlier studies, we demonstrated that AGPs play important roles during ovule differentiation in Larix decidua Mill. The presented results encouraged us to carry out further studies focused on the functions of these unique glycoproteins during pollen/pollen tube and ovule interactions in Larix. We identified and analyzed the localization of AGPs epitopes by JIM4, JIM8, JIM13 and LM2 antibodies (Abs) in male gametophytes and ovule tissue during pollination, the progamic phase, and after fertilization and in vitro growing pollen tubes. Our results indicated that (1) AGPs recognized by JIM4 Abs play an essential role in the interaction of male gametophytes and ovules because their appearance in ovule cells is induced by physical contact between reproductive partners; (2) after pollination, AGPs are secreted from the pollen cytoplasm into the pollen wall and contact the extracellular matrix of stigmatic tip cells followed by micropylar canal cells; (3) AGPs synthesized in nucellus cells before pollen grain germination are secreted during pollen tube growth into the extracellular matrix, where they can directly interact with male gametophytes; (4) in vitro cultured pollen tube AGPs labeled with LM2 Abs participate in the germination of pollen grain, while AGPs recognized by JIM8 Abs are essential for pollen tube tip growth.

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Arabinogalactan proteins: Distribution during the development of male and female gametophytes

Cited by 29 publications

References 86 publications

CRISPR-Cas9 multiplex genome editing of the hydroxyproline-O-galactosyltransferase gene family alters arabinogalactan-protein glycosylation and function in Arabidopsis

CRISPR-Cas9 multiplex genome editing of the hydroxyproline-O-galactosyltransferase gene family alters arabinogalactan-protein glycosylation and function in Arabidopsis

FLA14 is required for pollen development and preventing premature pollen germination under high humidity in Arabidopsis

Spatial and Temporal Distribution of Arabinogalactan Proteins during Larix decidua Mill. Male Gametophyte and Ovule Interaction

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