A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm

Lamport, Derek T. A.; Li, Tan; Kieliszewski, Marcia J.

doi:10.3390/cells10081935

Cited by 13 publications

(7 citation statements)

References 79 publications

(106 reference statements)

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“…This review recapitulates recent significant progress in AGP biology represented by the molecular pinball machine of the plasma membrane that unifies proton pumps, AGPs and Ca 2+ signalling [50].…”

Section: Final Conclusionmentioning

confidence: 89%

The Growth Oscillator and Plant Stomata: an Open and Shut Case

Lamport¹

2023

Preprint

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Since Darwin’s “Power of movement in plants” the precise mechanism of oscillatory plant growth remains elusive. Hence the search continues for the hypothetical growth oscillator that regulates a huge range of growth phenomena ranging from circumnutation to pollen tube tip growth and stomatal movements. Oscillators are essentially simple devices with few components. A universal growth oscillator with only four major components became apparent recently with the discovery of a missing component, notably arabinogalactan glycoproteins (AGPs) that store dynamic Ca2+ at the cell surface. Demonstrably, auxin-activated proton pumps, AGPs, Ca2+ channels and auxin efflux “PIN” proteins, embedded in the plasma membrane, combine to generate cytosolic Ca2+ oscillations that ultimately regulate oscillatory growth: Hechtian adhesion of the plasma membrane to the cell wall and auxin-activated proton pumps trigger the release of dynamic Ca2+ stored in periplasmic AGP monolayers. These four major components represent a molecular PINball machine a strong visual metaphor that also recognizes auxin efflux “PIN” proteins as an essential component. Proton “pinballs” dissociate Ca2+ ions bound by paired glucuronic acid residues of AGP glycomodules, hence reassesses the role of proton pumps. It shifts the prevalent paradigm away from the recalcitrant “acid growth” theory that proposes direct action on cell wall properties, with an alternative explanation that connects proton pumps to Ca2+ signaling with dynamic Ca2+ storage by AGPs, auxin transport by auxin-efflux PIN proteins and Ca2+ channels. The extensive Ca2+ signalling literature of plants ignores arabinogalactan proteins (AGPs). Such scepticism leads us to reconsider the validity of the universal growth oscillator proposed here with some exceptions that involve marine plants and perhaps the most complex stress-test, stomatal regulation.

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Section: Final Conclusionmentioning

confidence: 89%

The Growth Oscillator and Plant Stomata: an Open and Shut Case

Lamport¹

2023

Preprint

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“…Receptor-like protein kinases (RLKs) are a large family of membrane proteins essential for reproductive development (Cui et al, 2022), and Ca 2+ is described as an important ion in the entire reproductive process and has also been related to the putative functions and mode of action of AGPs (Cheng et al, 2002;Lamport and Vaŕnai, 2013). A recent study clearly highlighted AGPs as essential players involved in novel molecular pinball machines of the plasma membrane controlling cytosolic Ca 2+ levels that regulate plant metabolism (Lamport et al, 2021). In addition, recent studies have revealed that the capacity of AGPs to bind Ca 2+ ions is conferred by GlcA residues in the AGPs sugar chains (Lopez-Hernandez et al, 2020;Pfeifer et al, 2020;Zhang et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…Mutants of glucuronosyltransferases (GLCATs), responsible for the addition of glucuronic acid (GlcA) to the AGP sugar chains were developmentally defective due to the reduced Ca 2+ binding to GlcA residues of AGPs (Lopez-Hernandez et al, 2020;Zhang et al, 2020). Recently, a review by Lamport et al (2021) clearly points AGPs as essential players in controlling cytosolic Ca 2+ levels in the plasma membrane and regulating plant metabolism.…”

Section: Introductionmentioning

confidence: 99%

New insights on the expression patterns of specific Arabinogalactan proteins in reproductive tissues of Arabidopsis thaliana

et al. 2022

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Arabinogalactan proteins (AGPs) are hydroxyproline-rich glycoproteins containing a high proportion of carbohydrates, widely distributed in the plant kingdom and ubiquitously present in land plants. AGPs have long been suggested to play important roles in plant reproduction and there is already evidence that specific glycoproteins are essential for male and female gametophyte development, pollen tube growth and guidance, and successful fertilization. However, the functions of many of these proteins have yet to be uncovered, mainly due to the difficulty to study individual AGPs. In this work, we generated molecular tools to analyze the expression patterns of a subgroup of individual AGPs in different Arabidopsis tissues, focusing on reproductive processes. This study focused on six AGPs: four classical AGPs (AGP7, AGP25, AGP26, AGP27), one AG peptide (AGP24) and one chimeric AGP (AGP31). These AGPs were first selected based on their predicted expression patterns along the reproductive tissues from available RNA-seq data. Promoter analysis using β-glucuronidase fusions and qPCR in different Arabidopsis tissues allowed to confirm these predictions. AGP7 was mainly expressed in female reproductive tissues, more precisely in the style, funiculus, and integuments near the micropyle region. AGP25 was found to be expressed in the style, septum and ovules with higher expression in the chalaza and funiculus tissues. AGP26 was present in the ovules and pistil valves. AGP27 was expressed in the transmitting tissue, septum and funiculus during seed development. AGP24 was expressed in pollen grains, in mature embryo sacs, with highest expression at the chalazal pole and in the micropyle. AGP31 was expressed in the mature embryo sac with highest expression at the chalaza and, occasionally, in the micropyle. For all these AGPs a co-expression analysis was performed providing new hints on its possible functions. This work confirmed the detection in Arabidopsis male and female tissues of six AGPs never studied before regarding the reproductive process. These results provide novel evidence on the possible involvement of specific AGPs in plant reproduction, as strong candidates to participate in pollen-pistil interactions in an active way, which is significant for this field of study.

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“…Calcium is a crucial molecule in reproductive processes, and over the years the association between calcium and AGPs has been increasingly studied. A review from Lamport and collaborators highlighted AGPs as essential players involved in novel pinball machine-like structures in the plasma membrane controlling cytosolic calcium levels and regulating plant metabolism (Lamport et al, 2021). Given that many of the reproductive events are dependent on calcium oscillations, it is possible that some specific AGPs expressed throughout the reproductive tissues act in calcium-mediated signaling pathways (Figure 9) (Iwano et al, 2004(Iwano et al, , 2012.…”

Section: Galt25789 Mutant Agps Have Low Glucuronic Acid Contentmentioning

confidence: 99%

Type II arabinogalactans initiated by hydroxyproline‐O‐galactosyltransferases play important roles in pollen–pistil interactions

et al. 2023

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SUMMARY Arabinogalactan‐proteins (AGPs) are hydroxyproline‐rich glycoproteins containing a high sugar content and are widely distributed in the plant kingdom. AGPs have long been suggested to play important roles in sexual plant reproduction. The synthesis of their complex carbohydrates is initiated by a family of hydroxyproline galactosyltransferase (Hyp‐GALT) enzymes which add the first galactose to Hyp residues in the protein backbone. Eight Hyp‐GALT enzymes have been identified so far, and in the present work a mutant affecting five of these enzymes (galt2galt5galt7galt8galt9) was analyzed regarding the reproductive process. The galt25789 mutant presented a low seed set, and reciprocal crosses indicated a significant female gametophytic contribution to this mutant phenotype. Mutant ovules revealed abnormal callose accumulation inside the embryo sac and integument defects at the micropylar region culminating in defects in pollen tube reception. In addition, immunolocalization and biochemical analyses allowed the detection of a reduction in the amount of glucuronic acid in mutant ovary AGPs. Dramatically low amounts of high‐molecular‐weight Hyp‐O‐glycosides obtained following size exclusion chromatography of base‐hydrolyzed mutant AGPs compared to the wild type indicated the presence of underglycosylated AGPs in the galt25789 mutant, while the monosaccharide composition of these Hyp‐O‐glycosides displayed no significant changes compared to the wild‐type Hyp‐O‐glycosides. The present work demonstrates the functional importance of the carbohydrate moieties of AGPs in ovule development and pollen–pistil interactions.

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A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm

Cited by 13 publications

References 79 publications

The Growth Oscillator and Plant Stomata: an Open and Shut Case

The Growth Oscillator and Plant Stomata: an Open and Shut Case

New insights on the expression patterns of specific Arabinogalactan proteins in reproductive tissues of Arabidopsis thaliana

Type II arabinogalactans initiated by hydroxyproline‐O‐galactosyltransferases play important roles in pollen–pistil interactions

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