A two-way molecular dialogue between embryo and endosperm is required for seed development

Doll, Nicolas M.; Royek, Stefanie; Fujita, Satoshi; Okuda, Satoshi; Chamot, Sophy; Stintzi, Annick; Widiez, Thomas; Hothorn, Michael; Schaller, Andreas; Geldner, Niko; Ingram, Gwyneth

doi:10.1126/science.aaz4131

Cited by 112 publications

(122 citation statements)

References 39 publications

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“…We may thus expect that many different proteases with different specificities for cleavage site selection are required for the processing of the many different precursors. Consistent with this notion, precursor processing enzymes have been identified in different classes of proteases, including a metacaspase and a papain-like enzyme among the cysteine peptidases (Wrzaczek et al, 2015;Ziemann et al, 2018;Hander et al, 2019), a carboxypeptidase in the class of the zink-dependent metallo peptidases (Casamitjana-Martıńez et al, 2003), and several subtilases (SBTs) among the serine peptidases (Srivastava et al, 2009;Engineer et al, 2014;Ghorbani et al, 2016;Schardon et al, 2016;Stegmann et al, 2017;Beloshistov et al, 2018;Doll et al, 2020). SBTs thus seem to play a more general role in peptide hormone maturation .…”

Section: Introductionmentioning

confidence: 91%

The biogenesis of CLEL peptides involves several processing events in consecutive compartments of the secretory pathway

Stührwohldt

Scholl

Lang

et al. 2018

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AbstractPost-translationally modified peptides are involved in many aspects of plant growth and development. The maturation of these peptides from their larger precursors is still poorly understood. We show here that the biogenesis of CLEL6 and CLEL9 peptides in Arabidopsis thaliana requires a series of processing events in consecutive compartments of the secretory pathway. Following cleavage of the signal peptide upon entry into the endoplasmic reticulum (ER), the peptide precursors are processed in the cis-Golgi by the subtilase SBT6.1. SBT6.1-mediated cleavage within the variable domain allows for continued passage of the partially processed precursors through the secretory pathway, and is a prerequisite for subsequent post-translational modifications including tyrosine sulfation and proline hydroxylation within, and proteolytic maturation after exit from the Golgi. Activation by subtilase SBT3.8 in post-Golgi compartments depends on the N-terminal aspartate of the mature peptides. Our work highlights the complexity of post-translational precursor maturation allowing for stringent control of peptide biogenesis.

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Section: Introductionmentioning

confidence: 91%

The biogenesis of CLEL peptides involves several processing events in consecutive compartments of the secretory pathway

Stührwohldt

Scholl

Lang

et al. 2018

Preprint

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“…Strikingly, the number of epicuticular wax crystals was considerably reduced and wax crystals appeared smaller in ad1 mutant leaves than wild type ( Figure 3B). We also quantified the accumulation of toluidine blue stain in germinating coleoptiles, an assay used to measure cuticle permeability, and detected a higher accumulation of the dye in ad1 mutants ( Figure 3C,D), suggesting defects in cuticle formation during embryogenesis (Tanaka et al, 2004;Doll et al, 2020). In addition, we also examined cuticular wax accumulation by measuring cuticular transpiration and chlorophyll leaching ( Figure 3E,F), which are frequently used to examine cuticular defects in leaves (Chen et al, 2003).…”

Section: Cuticular Wax Biosynthesis and Deposition Are Defective In Amentioning

confidence: 99%

“…For assessing cuticle integrity, toluidine blue tests were performed, as previously described (Tanaka et al, 2004;Doll et al, 2020). Two-day old etiolated coleoptiles were stained for 5 minutes in a toluidine blue solution (0.05% w/v) with Tween 20 (0.1% v/v) and washed in tap water.…”

Section: Toluidine Blue Permeability Testmentioning

confidence: 99%

“…Detailed characterization of various organ fusion mutants in early stages of development should improve understanding of the molecular and cellular mechanics of how the cuticle suppresses epidermal fusion in plants. For example, recent work in Arabidopsis revealed mechanistic details of the early steps of cuticle deposition by the action of an endosperm localized subtilase and peptide/receptor complexes derived from the embryo(Doll et al, 2020).…”

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confidence: 99%

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The FUSED LEAVES1/ADHERENT1Regulatory Module Is Required For Maize Cuticle Development And Organ Separation

Liu

Bourgault

Strable

et al. 2020

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ORCID IDs: 0000-0002-9928-7114 (X.Liu); 0000-0002-0260-8285 (J. Strable); 0000-0002-1901-2971 (A. Gallavotti) Running title: maize cuticle formationOne sentence summary: The classic maize mutant adherent1, first isolated a century ago, is affected in an enzyme responsible for cuticle formation that is regulated by the MYB transcription factor FUSED LEAVES1. ABSTRACTIn land plants all aerial epidermal cells are covered by the cuticle, an extracellular hydrophobic layer. The cuticle represents a primary barrier between cells and the 4 Cutin is a polyester matrix composed mainly of glycerol and long-chain (C16

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“…Recently, the Hothorn group identified the molecular mechanism of SGN3-CIF2 binding by producing a crystal structure of SGN3 . A surveillance pathway involving SGN3 and another receptor-like kinase, GASSHO2, was also shown to safeguard the integrity of the embryonic cuticle by interacting with the sulfated peptide ligand TWISTED SEED 1 Ó 2020 The Authors New Phytologist Ó 2020 New Phytologist Trust www.newphytologist.com Forum (Doll et al, 2020). Therefore, the same receptor-like kinase evolved distinct integrity monitoring functions within the plant.…”

Section: Membrane Signalingmentioning

confidence: 99%

ROS production by localized SCHENGEN receptor module drives lignification at subcellular precision

Fujita

et al. 2019

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26Production of reactive-oxygen species (ROS) by NADPH oxidases (NOXs) impacts many 27 processes in animals and plants and many plant receptor pathways involve rapid, NOX-dependent 28 increases of ROS. Yet, their general reactivity has made it challenging to pinpoint the precise role 29 and direct cellular targets of ROS. A well-understood ROS target in plants are lignin peroxidases 30 in the cell wall. Lignin can be deposited with exquisite spatial control, but the underlying 31 mechanisms have remained elusive. Here we establish a full kinase signaling relay that exerts 32 direct, spatial control over ROS production and lignification within the cell wall. We show that 33 polar localization of a single kinase component is crucial for pathway function. Our data indicates 34 that an intersection of more broadly localized components allows for micrometer-scale precision 35 of lignification and that this system is triggered through initiation of ROS production as a critical 36 peroxidase co-substrate. 37 As in animals, NADPH oxidase-produced ROS in plants is important for a multitude of 38 processes and the number of NADPH oxidase genes (10 in Arabidopsis, called RESPIRATORY 39 BURST OXIDASE HOMOLOGs, RBOHs, A-J) suggests a high complexity of regulation of ROS 40 production in plants. Among its many roles, ROS-dependent regulation of plant cell wall structure and 41 function is considered to be among its most critical 1 . The cell wall is the nano-structured, sugar-based, 42 2 pressure-resisting extracellular matrix of plants and NOXs are thought to be the predominant ROS 43 source in this compartment (also termed apoplast) 1 . 44A staggering number of kinases have been shown to regulate plant NOXs and the activation 45 mechanism of NOX-dependent ROS production is well established, especially in response to microbial 46 pattern-recognition by immune receptors 2 . However, the specific role and direct molecular targets of 47 ROS during microbial pattern-recognition have remained elusive 3 . The same applies for the central 48 role of ROS in tip growing cells, such as root hairs or pollen tubes, where ROS is thought to be part of 49 an intricate oscillation of cell wall stiffening and loosening, aimed at allowing cell wall expansion 50 without catastrophic collapse 4,5 . In this case, ROS is proposed to be important for counteracting cell 51 wall loosening pH decreases, but it is again unclear what direct targets of ROS would mediate cell wall 52 stiffening. Cell wall lignification by apoplastic peroxidases, can therefore be considered as the most 53 well-established role of ROS, where the peroxidases themselves are the direct "ROS targets", using it 54 as a co-substrate for the oxidation of mono-lignols 6,7 . In the case of lignification, however, a 55 molecularly-defined signaling pathway that induces ROS production during lignification has not been 56 defined. A few years ago, our group identified a specific NADPH oxidase, RBOHF, to be required for 57 the localized formation of lignin in the root end...

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A two-way molecular dialogue between embryo and endosperm is required for seed development

Cited by 112 publications

References 39 publications

The biogenesis of CLEL peptides involves several processing events in consecutive compartments of the secretory pathway

The biogenesis of CLEL peptides involves several processing events in consecutive compartments of the secretory pathway

The FUSED LEAVES1/ADHERENT1Regulatory Module Is Required For Maize Cuticle Development And Organ Separation

ROS production by localized SCHENGEN receptor module drives lignification at subcellular precision

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