EXPANSIN A1-mediated radial swelling of pericycle cells positions anticlinal cell divisions during lateral root initiation

Ramakrishna, Priya; Duarte, Perla Alcaraz; Rance, Graham A.; Schubert, Martin; Vordermaier, Vera; Vu, Lam Dai; Murphy, Evan; Barro, Amaya Vilches; Swarup, Kamal; Moirangthem, Kamaljit; Jørgensen, Bodil; Cotte, Brigitte van de; Goh, Tatsuaki; Lin, Zhefeng; Voβ, Ute; Beeckman, Tom; Bennett, Malcolm; Gevaert, Kris; Maizel, Alexis; Smet, Ive De

doi:10.1073/pnas.1820882116

Cited by 77 publications

(82 citation statements)

References 57 publications

(94 reference statements)

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“…All of these diverse organisms are confronted with the dilemma of how to loosen their cellulose-based matrix of structural carbohydrates in order to expand their cell walls during normal growth and development. In plants and some green algae, nonenzymatic proteins called expansins provide the most important functions for loosening structural cellulose, and expansins are most highly expressed during active growth in any tissue where cell wall extension is critical (Brummell et al, 1999;Chen & Bradford, 2000;Cho & Cosgrove, 2000;Im et al, 2000;Pien et al, 2001;Lee et al, 2003;Gray-Mitsumune et al, 2004;Cosgrove, 2016;Ramakrishna et al, 2019). Expansin proteins are tightly packed two-domain structures of 200-250 amino acids with a planar polysaccharide binding surface (Supporting Information Fig.…”

Section: Introductionmentioning

confidence: 99%

Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution

et al. 2020

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Summary Plants must rearrange the network of complex carbohydrates in their cell walls during normal growth and development. To accomplish this, all plants depend on proteins called expansins that nonenzymatically loosen noncovalent bonding between cellulose microfibrils. Surprisingly, expansin genes have more recently been found in some bacteria and microbial eukaryotes, where their biological functions are largely unknown. Here, we reconstruct a comprehensive phylogeny of microbial expansin genes. We find these genes in all eukaryotic microorganisms that have structural cell wall cellulose, suggesting expansins evolved in ancient marine microorganisms long before the evolution of land plants. We also find expansins in an unexpectedly high diversity of bacteria and fungi that do not have cellulosic cell walls. These bacteria and fungi inhabit varied ecological contexts, mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell walls are present. The microbial expansin phylogeny shows evidence of multiple horizontal gene transfer events within and between bacterial and eukaryotic microbial lineages, which may in part underlie their unusually broad phylogenetic distribution. Overall, expansins are unexpectedly widespread in bacteria and eukaryotes, and the contribution of these genes to microbial ecological interactions with plants and algae has probbaly been underappreciated.

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Section: Introductionmentioning

confidence: 99%

Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution

et al. 2020

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“…A widely accepted (textbook) explanation invokes low pH-dependent wall loosening "enzymes" and Proton extrusion and a concomitantly low wall pH associated with cell extension so-called "acid growth" [41] exemplify Lord Rutherford's dictum that "No experimental result is ever wrong." A widely accepted (textbook) explanation invokes low pH-dependent wall loosening "enzymes" and expansins all of unknown specificity [42] but ignores the dissociation of AGP-Ca 2+ that provides an alternative reinterpretation of "acid growth" based on a visual analogy of the plasma membrane depicted as a metaphorical "molecular pin-ball machine" in (Supplemental Data) that regulates three ion fluxes, H + , Ca 2+ and auxin (anions at neutral pH, neutral at low pH). When activated by auxin, the proton pump shoots fast protons into the periplasm where they dislodge Ca 2+ ions from the periplasmic AGP glycomodules; i.e., proton efflux generates Ca 2+ influx.…”

Section: A Molecular Pin-ball Machine Regulates Ion Fluxes At the Plamentioning

confidence: 99%

Phyllotaxis Turns Over a New Leaf—A New Hypothesis

Lamport

Held

et al. 2020

IJMS

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Phyllotaxis describes the periodic arrangement of plant organs most conspicuously floral. Oscillators generally underlie periodic phenomena. A hypothetical algorithm generates phyllotaxis regulated by the Hechtian growth oscillator of the stem apical meristem (SAM) protoderm. The oscillator integrates biochemical and mechanical force that regulate morphogenetic gradients of three ionic species, auxin, protons and Ca 2+ . Hechtian adhesion between cell wall and plasma membrane transduces wall stress that opens Ca 2+ channels and reorients auxin efflux "PIN" proteins; they control the auxin-activated proton pump that dissociates Ca 2+ bound by periplasmic arabinogalactan proteins (AGP-Ca 2+ ) hence the source of cytosolic Ca 2+ waves that activate exocytosis of wall precursors, AGPs and PIN proteins essential for morphogenesis. This novel approach identifies the critical determinants of an algorithm that generates phyllotaxis spiral and Fibonaccian symmetry: these determinants in order of their relative contribution are: (1) size of the apical meristem and the AGP-Ca 2+ capacitor; (2) proton pump activity; (3) auxin efflux proteins; (4) Ca 2+ channel activity; (5) Hechtian adhesion that mediates the cell wall stress vector. Arguably, AGPs and the AGP-Ca 2+ capacitor plays a decisive role in phyllotaxis periodicity and its evolutionary origins.Int. J. Mol. Sci. 2020, 21, 1145 2 of 15 stress-strain to the plasma membrane where an auxin-activated proton pump dissociates AGP-Ca 2+ . Elevated cytosolic Ca 2+ -activates exocytosis thus regulating plant growth. Discussion of the Hechtian Oscillator vis-a-vis the role of the primary cell wall in plant morphogenesis [2] suggests extrapolating the oscillator to phyllotaxis based on the premise that presence of the oscillator components implies the presence of a functional Hechtian Oscillator. Indeed, recent work suggests the mechanotransduction of stress relocates auxin efflux PIN proteins that generate new protoderm primordia. However, the precise biochemical mechanisms involved in stress transduction and the role of auxin and calcium homeostasis remain to be elucidated. Here, we invoke Hechtian adhesion and AGPs as essential components that lead us to propose a novel biochemical algorithm for floral phyllotaxis and an explanation of its strong tendency towards a periodic series first described by Fibonacci (1170Fibonacci ( -1240. This approach contrasts with many previous studies with an overwhelming mathematical bias. Indeed, many observations in Nature involve periodicity and the probable underlying oscillations Oscillatory plant growth, known since Darwin [3], was subsequently confirmed by rapid tip growth of pollen tubes and root hairs [4]. Plant morphogenesis also involves periodicity strikingly displayed by the pattern of leaves and floral organs [5] that often appear as Fibonacci spirals typified by whorls of 3, 5, 8, 13, 21 and 34 petals [6]. Hypothetically, such periodicity depends on an underlying oscillator such as the recently formulated Hechtian growth oscilla...

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“…phyllotaxis is a test case of the Hechtian oscillator and its general applicability developed in the following sections: [39] Proton extrusion and a concomitantly low wall pH associated with cell extension socalled "acid growth" [41] exemplifies Lord Rutherford's dictum that "No experimental result is ever wrong." A widely accepted (textbook) explanation invokes low pH-dependent wall loosening "enzymes" and expansins all of unknown specificity [42] but ignore dissociation of AGP-Ca 2+ that provides an alternative reinterpretation of "acid growth" based on a visual analogy of the plasma membrane depicted as a metaphorical "molecular pin-ball machine" in (Supplement S1) that regulates three ion fluxes, H + , Ca 2+ and auxin (anions at neutral pH, neutral at low pH). When activated by auxin the proton pump shoots fast protons into the periplasm where they dislodge Ca 2+ ions from the periplasmic AGP glycomodules; i.e.…”

Section: Auxin Activity Is a Proxy For The Hechtian Oscillatormentioning

confidence: 99%

Phyllotaxis Turns over a New Leaf – A Review<strong> </strong>

Lamport¹,

Li²,

Held³

et al. 2019

Preprint

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Sixty years ago in the lab adjacent to Fred Sanger (1958 Nobel Prize for protein chemistry), I discovered the cell surface hydroxyproline-rich glycoproteins. Nature keeps some of her secrets longer than others. It has taken many years to dissect the molecular function and biological role of extensins and arabinogalactan proteins (AGPs). Extensins template the formation of new cell walls. AGPs remained baffling and enigmatic until a Eureka moment when computer prediction of AGP calcium binding depicted paired glucuronic acid residues and thus the likely role of a cell surface AGP-Ca2+capacitor: In conjunction with the auxin-activated proton pump that releases bound Ca2+ it led us to formulate the Hechtian Growth Oscillator as A Global Paradigm with a pivotal role in Ca2+ homeostasis. The ramifications are profound. They cannot be shrugged off with sceptical disdain but demand critical reappraisal of current dogma. Phyllotaxis is an ancient problem; it involves an essential role for auxin and the auxin efflux “PIN” proteins together with mechanotransduction of stress-strain as phyllotactic determinants. However, a general explanation remains elusive despite much effort, particularly by mathematicians. Here we propose a novel biochemical algorithm: Hechtian oscillator transduction of cell wall stress generates phyllotactic patterns quite independent of a mathematical approach. Plants simply use different rules and follow a different route.

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EXPANSIN A1-mediated radial swelling of pericycle cells positions anticlinal cell divisions during lateral root initiation

Cited by 77 publications

References 57 publications

Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution

Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution

Phyllotaxis Turns Over a New Leaf—A New Hypothesis

Phyllotaxis Turns over a New Leaf – A Review<strong> </strong>

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EXPANSIN A1-mediated radial swelling of pericycle cells positions anticlinal cell divisions during lateral root initiation

Cited by 77 publications

References 57 publications

Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution

Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution

Phyllotaxis Turns Over a New Leaf—A New Hypothesis

Phyllotaxis Turns over a New Leaf &ndash; A Review<strong> </strong>

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Phyllotaxis Turns over a New Leaf – A Review<strong> </strong>