ZHOUPI and KERBEROS Mediate Embryo/Endosperm Separation by Promoting the Formation of an Extracuticular Sheath at the Embryo Surface

Moussu, Steven; Doll, Nicolas M.; Chamot, Sophy; Brocard, Lysiane; Creff, Audrey; Fourquin, Chloé; Widiez, Thomas; Nimchuk, Zachary L.; Ingram, Gwyneth

doi:10.1105/tpc.17.00016

Cited by 56 publications

(67 citation statements)

References 40 publications

(73 reference statements)

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“…Since all gso1-1 gso2-1 mutant seeds are twisted, non-additivity cannot be concluded from this phenotype. However, recent work has shown that additivity of toluidine blue staining phenotypes can be detected in mutant combinations with gso1-1 gso2-1 [41]. The frequency of “twisted” seeds (including ruptured seeds), and toluidine blue stained seedling cotyledons was non-additive in ale1-4 mpk6-2 double mutant plants, consistent with ALE1, GSO1, GSO2 and MPK6 acting in the same genetic pathway to control seedling cotyledon permeability (Figure 6 and Supplementary Figure 10).…”

Section: Resultsmentioning

confidence: 99%

A stress-response-related inter-compartmental signalling pathway regulates embryonic cuticle integrity in Arabidopsis

Creff

Brocard

Joubès

et al. 2018

Preprint

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22The embryonic cuticle is necessary for normal seed development and seedling establishment 23 in Arabidopsis. Although mutants with defective embryonic cuticles have been identified, 24 neither the deposition of cuticle material, nor its regulation, has been described during 25 embryogenesis. Here we use electron microscopy, lipid staining and permeability assays to 26 show that cuticle deposition initiates de novo in patches on globular embryos. By combining 27 these techniques with genetics and gene expression analysis, we show that successful patch 28 coalescence to form a continuous cuticle requires a signalling involving the endosperm-29 specific subtilisin protease ALE1 and the receptor kinases GSO1 and GSO2, which are 30 expressed in the developing embryonic epidermis. Transcriptome analysis shows that this 31 pathway regulates stress-related gene expression in seeds. Consistent with these findings we 32 show genetically, and through activity analysis, that the stress-associated MPK6 protein acts 33 downstream of GSO1 and GSO2 in the developing embryo. We propose that a stress-34 related signalling pathway has been hijacked in some angiosperm seeds through the 35 recruitment of endosperm-specific components. Our work reveals the presence of an inter-36 compartmental dialogue between the endosperm and embryo that ensures the formation of 37 an intact and functional cuticle around the developing embryo through an "auto-immune" 38 type interaction. 39 40 41 endosperm breaks down, leaving space for the growing embryo. By the end of seed development, 46 only a single endosperm cell layer envelops the embryonic tissues (reviewed in [1]).47 48 The endosperm is an angiosperm innovation, thought to have arisen through the 49 sexualisation of the central cell of the female gametophyte [2]. The ancestors of angiosperms 50 probably had seeds more similar to those of gymnosperms, in which tissues of the female 51 gametophyte proliferate independently of egg cell fertilization to produce a nutrient rich storage 52 tissue. However, the endosperm plays not only a nutritional role, but also a role in regulating 53 embryo development. For example, the peptide CLAVATA3/EMBRYO SURROUNDING 54 REGION-RELATED8 (CLE8) may act non-cell autonomously to regulate early Arabidopsis 55 embryogenesis [3]. Recently, maternally-expressed peptides present in the central cell pre-56 fertilization, and subsequently in the early EMBRYO SURROUNDING REGION (ESR), were 57 shown to regulate Arabidopsis suspensor development. Genetic analysis suggests that this 58 regulation could be mediated by a pathway involving the Receptor-Like Cytoplasmic Kinase 59 SHORT SUSPENSOR [4,5], although the receptor involved remains unidentified.60 61In previous works we showed genetically that the ESR-specific subtilisin protease 62 Abnormal LEaf-shape1 (ALE1) acts in the same genetic pathway as two embryonically-expressed 63 receptor kinases, GASSHO1 [(GSO1) also known as SCHENGEN3 [6]] and GASSHO2 (GSO2), 64 to control the formation of the embryonic...

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Section: Resultsmentioning

confidence: 99%

A stress-response-related inter-compartmental signalling pathway regulates embryonic cuticle integrity in Arabidopsis

Creff

Brocard

Joubès

et al. 2018

Preprint

Self Cite

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“…The krs mutants fail to form the gap between the embryo and the endosperm, demonstrating the significant function of the KRS peptide in tissue separation. When the krs seeds germinate, the abnormally expanded cup‐shaped cotyledons are observed (Moussu et al ). These results suggest that the separation of the embryo and the endosperm during seed development is an essential preparation for seed germination.…”

Section: Seed Germinationmentioning

confidence: 99%

“…In developing Arabidopsis seeds, cutin is deposited on the surface of the embryo as well (Moussu et al 2017) ( Figure 3D). Mutations in ZHOUPI/RETARDED GROWTH OF EMBRYO 1 (ZOU/RGE1), an endospermspecific bHLH transcription factor (Kondou et al 2008;Yang et al 2008), cause defective cutin deposition in the embryo and result in the adhesion of the embryonic surface to the endospermic cells (Tanaka et al 2001;Yang et al 2008).…”

Section: Endosperm-embryo Interphase à a Previously Unrecognized Layermentioning

confidence: 99%

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Seed germination and dormancy: The classic story, new puzzles, and evolution

Nonogaki¹

2019

JIPB

133

141

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This review highlights recent progresses in seed germination and dormancy research. Research on the weakening of the endosperm during germination, which is almost a classic theme in seed biology, was resumed by α‐xylosidase studies. Strong genetic evidence was presented to suggest that the quality control of xyloglucan biosynthesis in the endosperm (and the embryo) plays a critical role in germination. Further analyses on the endosperm and the adjacent layers have suggested that the cutin coat in the endosperm‐testa interphase negatively affects germination while the endosperm‐embryo interphase produces a sheath that facilitates germination. These progresses significantly advanced our understanding of seed germination mechanisms. A breakthrough in dormancy research, on the other hand, revealed the unique abscisic acid signaling pathway that is regulated by DELAY OF GERMINATION1 (DOG1). The detailed analysis of DOG1 expression uncovered the intriguing story of reciprocal regulation of the sense‐antisense pair, which generated new questions. Recent studies also suggested that the DOG1 function is not limited to dormancy but extended through general seed maturation, which provokes questions about the evolution of DOG1 family proteins. Seed biology is becoming more exciting with the classic stories being revitalized and new puzzles emerging from the frontier.

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“…When null alleles are not available, alternative methods can be used to determine whether gene function is required for embryo development. One promising approach involves TALEN and/or CRISPR-Cas9-targeted gene inactivation (Moussu et al, 2017;Shin et al, 2018). This strategy should become even more widespread in the future.…”

Section: Reviewmentioning

confidence: 99%

Genome‐wide identification of EMBRYO‐DEFECTIVE (EMB) genes required for growth and development in Arabidopsis

Meinke

2019

New Phytologist

137

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Summary With the emergence of high‐throughput methods in plant biology, the importance of long‐term projects characterized by incremental advances involving multiple laboratories can sometimes be overlooked. Here, I highlight my 40‐year effort to isolate and characterize the most common class of mutants encountered in Arabidopsis (Arabidopsis thaliana): those defective in embryo development. I present an updated dataset of 510 EMBRYO‐DEFECTIVE (EMB) genes identified throughout the Arabidopsis community; include important details on 2200 emb mutants and 241 pigment‐defective embryo (pde) mutants analyzed in my laboratory; provide curated datasets with key features and publication links for each EMB gene identified; revisit past estimates of 500–1000 total EMB genes in Arabidopsis; document 83 double mutant combinations reported to disrupt embryo development; emphasize the importance of following established nomenclature guidelines and acknowledging allele history in research publications; and consider how best to extend community‐based curation and screening efforts to approach saturation for this diverse class of mutants in the future. Continued advances in identifying EMB genes and characterizing their loss‐of‐function mutant alleles are needed to understand genotype‐to‐phenotype relationships in Arabidopsis on a broad scale, and to document the contributions of large numbers of essential genes to plant growth and development.

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ZHOUPI and KERBEROS Mediate Embryo/Endosperm Separation by Promoting the Formation of an Extracuticular Sheath at the Embryo Surface

Cited by 56 publications

References 40 publications

A stress-response-related inter-compartmental signalling pathway regulates embryonic cuticle integrity in Arabidopsis

A stress-response-related inter-compartmental signalling pathway regulates embryonic cuticle integrity in Arabidopsis

Seed germination and dormancy: The classic story, new puzzles, and evolution

Genome‐wide identification of EMBRYO‐DEFECTIVE (EMB) genes required for growth and development in Arabidopsis

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