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Seed Development

Personnel du RDP

Gwyneth INGRAM

gwyneth.ingram
(33) 4 26 23 39 78
DR2 CNRS

Peter ROGOWSKY

Peter.Rogowsky
(33) 4 72 72 86 07
DR1 INRA

Thomas WIDIEZ

thomas.widiez
(33) 4 72 72 86 08
CR1 INRA

Nathalie DEPEGE-FARGEIX

Nathalie.Depege
(33) 4 72 72 89 85
MC UCBL

Audrey CREFF

audrey.creff
(33) 4 72 72 89 85
IE CNRS

Jérome LAPLAIGE

jerome.laplaige
04 72 72 86 07
CDD IE INRA

Ghislaine GENDROT

ghislaine.gendrot
(33) 4 72 72 86 07
AI INRA

Christelle RICHARD

christelle.richard
(33) 4 72 72 85 91
CDD AI INRA

Edwige DELAHAYE

edwige.delahaye1
(33) 4 72 72 85 91
CDD AI INRA

Sophy CHAMOT

sophy.chamot
(33) 4 72 72 86 14
TCE CNRS

Anne Charlotte MARSOLLIER

AGPR

Douglas PYOTT

Postdoc

Laurine GILLES

laurine.gilles
04 72 72 39 59
Thèse

Nicolas DOLL

nicolas.doll
04 72 72 86 10
Thèse

Jeanne Loue MANIFEL

jeanne.loue-manifel
Thèse



2018


Lang D, Ullrich KK, Murat F, Fuchs J, Jenkins J, Haas FB, Piednoel M, Gundlach H, Van Bel M, Vives Cobo, Morata J, Symeonidi A, Hiss M, Meyberg R, Muchero W, Kamisugi Y, Saleh O, Blanc G, Decker EL, van Gessel N, Grimwood J, Hayes R, Graham SW, Gunter LE, McDaniel S, Hoernstein SNW, Larsson A, Li FW, Phillips J, Ranjan P, Rokshar DS, Rothfels CJ, Schneider L, Shu S, Stevenson DW, Thümmler F, Tillich M, Villarreal JCA, Widiez T, Wong GKS, Wymore A, Zhang Y, Zimmer AD, Quatrano RS, Mayer KFX, Goodstein D, Casacuberta JM, Vandepoele K, Reski R, Cuming AC, Tuskan J, Maumus F, Salse J, Schmutz J, Rensing SA. "The P. patens chromosome-scale assembly reveals moss genome structure and evolution". Plant Journal (2018)
PMID: 29237241

Darracq A, Vitte C, Nicolas S, Duarte J, Pichon JP, Mary-Huard T, Chevalier C, Bérard A, Le Paslier MC, Rogowsky P, Charcosset A, Joets J. "Sequence analysis of European maize inbred line F2 provides new insights into molecular and chromosomal characteristics of presence/absence variants". BMC Genomics. (2018)
PMID: 29402214

2017


"Ingram GC. Dying to live: cell elimination as...". (2017)
Ingram GC.
Dying to live: cell elimination as a developmental strategy in angiosperm seeds.
J Exp Bot. [PMID: 27702990]

"Meyer HM, Teles J, Formosa-Jordan P, Refahi...". (2017)
Meyer HM, Teles J, Formosa-Jordan P, Refahi Y, San-Bento R, Ingram G, Jönsson H, Locke JC, Roeder AH.
Fluctuations of the transcription factor ATML1 generate the pattern of giant cells in the Arabidopsis sepal
Elife. 2017 [PMID: 28145865]

"Doll MN, Depège-Fargeix N, Rogowsky PM, Widiez...". (2017)
Doll MN, Depège-Fargeix N, Rogowsky PM, Widiez T.
Signaling in early maize kernel development
Molecular Plant. 2017 [PMID: 28267956]

"Gilles LM, Khaled A, Laffaire JB, Chaignon S,...". (2017)
Gilles LM, Khaled A, Laffaire JB, Chaignon S, Gendrot G, Laplaige J, Bergès H, Beydon G, Bayle V, Barret P, Comadran J, Martinant JP, Rogowsky PM, Widiez T.
Loss of pollen-specific phospholipase NOT LIKE DAD triggers gynogenesis in maize
EMBO J. 2017 [PMID: 28228439]
Featured in EMBO J; INRA; CNRS; ENS de Lyon

"Amanda D, Doblin MS, Galletti R, Bacic A,...". (2017)
Amanda D, Doblin MS, Galletti R, Bacic A, Ingram GC, Johnson KL
Regulation of Cell Wall Genes in Response to DEFECTIVE KERNEL1 (DEK1)-Induced Cell Wall Changes.
Plant Signal Behav [PMID: 28692330]

"Moussu SA, Doll NM, Chamot S, Brocard L,...". (2017)
Moussu SA, Doll NM, Chamot S, Brocard L, Creff A, Fourquin C, Widiez T, Nimchuk ZL, Ingram GC.
ZHOUPI and KERBEROS Mediate Embryo/Endosperm Separation by Promoting the Formation of an Extra-Cuticular Sheath at the Embryo Eurface.
Plant Cell [PMID: 28696222]

"Ingram G, Nawrath C. The roles of the cuticle...". (2017)
Ingram G, Nawrath C. The roles of the cuticle in plant development: organ adhesions and beyond. J Exp Bot. [PMID: 28992283]

"Tran D, Galletti R, Neumann ED, Dubois A,...". (2017)
Tran D, Galletti R, Neumann ED, Dubois A, Sharif-Naeini R, Geitmann A, Frachisse JM, Hamant O, Ingram GC A mechanosensitive Ca2+ channel activity is dependent on the developmental regulator DEK1. Nat Commun. [PMID: 29044106]

"Gilles LM, Martinant JP, Rogowsky PM, Widiez...". (2017)
Gilles LM, Martinant JP, Rogowsky PM, Widiez T. Haploid induction in plants. Current Biology [PMID: 29065285]

"Widiez, T., Ingram, G. C. & Gutierrez-Marcos,...". (2017)
Widiez, T., Ingram, G. C. & Gutierrez-Marcos, J. Embryo-Endosperm-Sporophyte Interaction in Maize Seeds. in Maize Kernel Development 95–107 (Brian A. Larkins, 2017). [Link to the book]

"Amanda D, Doblin MS, MacMillan CP, Galletti...". (2017)
Amanda D, Doblin MS, MacMillan CP, Galletti R, Golz JF, Bacic A, Ingram GC, Johnson KL. Arabidopsis DEFECTIVE KERNEL1 regulates cell wall composition and axial growth in the inflorescence stem. Plant Direct [Link]

"Youssef D, Nihou A, Partier A, Tassy C, Paul...". (2017)
Youssef D, Nihou A, Partier A, Tassy C, Paul W, Rogowsky PM, Beckert M and Barret P. Induction of targeted deletions in transgenic bread wheat (Triticum aestivum L.) using customised meganuclease.
Plant Mol Biol Rep [Link to]

2016


"Delude C, Moussu S, Joubès J, Ingram G and...". (2016)
Delude C, Moussu S, Joubès J, Ingram G and Domergue F.
Plant surface lipids and epidermis development. Lipids in Plant and Algae Development. Subcell Biochem. [PMID: 27023240]

"Ingram G, Fujiwara T. Special Focus Issue on...". (2016)
Ingram G, Fujiwara T.
Special Focus Issue on Plant Responses to the Environment.
Plant Cell Physiol. [PMID: 2016 27091852]

"Fourquin C, Beauzamy L, Chamot S, Creff A,...". (2016)
Fourquin C, Beauzamy L, Chamot S, Creff A, Goodrich J, Boudaoud A, Ingram G.
Mechanical stress mediated by both endosperm softening and embryo growth underlies endosperm elimination in Arabidopsis seeds.
Development. [PMID: 27287798]

"Beauzamy L, Fourquin C, Dubrulle N, Boursiac...". (2016)
Beauzamy L, Fourquin C, Dubrulle N, Boursiac Y, Boudaoud A, Ingram G.
Endosperm turgor pressure decreases during early Arabidopsis seed development.
Development. [PMID: 27287811]

"Galletti R, Verger S, Hamant O, and Ingram G....". (2016)
Galletti R, Verger S, Hamant O, and Ingram G.
Developing a ‘thick skin’ : a paradoxical role for mechanical tension in maintaining epidermis integrity?
Development. [PMID: 27624830]

"Sucher J, Boni R, Yang P, Rogowsky P, Kumlehn...". (2016)
Sucher J, Boni R, Yang P, Rogowsky P, Kumlehn J, Krattinger SG, Keller B.
The durable wheat disease resistance gene Lr34 confers common rust and northern corn leaf blight resistance in maize. Plant Biotech J. [PMID: 27734576]

"Amanda D, Doblin MS, Galletti R, Bacic A,...". (2016)
Amanda D, Doblin MS, Galletti R, Bacic A, Ingram GC, Johnson KL.
DEFECTIVE KERNEL1 (DEK1) regulates cell walls in the leaf epidermis Plant Physiol. 2016 [PMID: 27756823]

2015


"Creff A, Brocard L, Ingram G. A mechanically...". (2015)
Creff A, Brocard L, Ingram G.
A mechanically sensitive cell layer regulates the physical properties of the Arabidopsis seed coat.
Nat Commun. 2015 [PMID: 25702924]

"Galletti R, Johnson KL, Scofield S, San-Bento...". (2015)
Galletti R, Johnson KL, Scofield S, San-Bento R, Watt AM, Murray JA, Ingram GC.
DEFECTIVE KERNEL 1 promotes and maintains plant epidermal differentiation. Development. 2015 [PMID: 25953348]

"McLaughlin JE, Bin-Umer MA, Widiez T, Finn D,...". (2015)
McLaughlin JE, Bin-Umer MA, Widiez T, Finn D, McCormick S, Tumer NE.
A Lipid Transfer Protein Increases the Glutathione Content and Enhances Arabidopsis Resistance to a Trichothecene Mycotoxin. [PMID: 26057253]

"Grimault A, Gendrot G, Chaignon S, Gilard F,...". (2015)
Grimault A, Gendrot G, Chaignon S, Gilard F, Tcherkez G, Thévenine J, Dubreucq B, Depège-Fargeix N, Rogowsky PM.
Role of B3 domain transcription factors of the AFL family in maize kernel filling. Plant Science. 2015 [PMID: 26025525]

"Grimault A, Gendrot G, Chaignon S, Gilard F,...". (2015)
Grimault A, Gendrot G, Chaignon S, Gilard F, Tcherkez G, Thévenine J, Dubreucq B, Depège-Fargeix N, Rogowsky PM.
Role of B3 domain transcription factors of the AFL family in maize kernel filling. Plant Science. 2015 [PMID: 26025525]

"La Rocca N, Manzotti PS, Cavaiuolo M,...". (2015)
La Rocca N, Manzotti PS, Cavaiuolo M, Barbante A, Dalla Vecchia F, Gabotti D, Gendrot G, Horner DS, Krstajic J, Persico M, Rascio N, Rogowsky P, Scarafoni A, Consonni G.
The maize fused leaves1 (fdl1) gene controls organ separation in the embryo and seedling shoot and promotes coleoptile opening.
J Exp Bot. 2015 [PMID: 26093144]

"Ingram G and Gutierrez-Marcos J. Peptide...". (2015)
Ingram G and Gutierrez-Marcos J.
Peptide signalling during angiosperm seed development.
J Exp Bot. 2015 [PMID: 26195729]

"Galletti R and Ingram GC. Communication is...". (2015)
Galletti R and Ingram GC.
Communication is key: reducing DEK1 activity reveals a link between cell-cell contacts and epidermal cell differentiation status.
Communicative & Integrative Biology, 2015 [PMID: 27064205]

"Grimault A, Gendrot G, Chamot S, Widiez T,...". (2015)
Grimault A, Gendrot G, Chamot S, Widiez T, Rabillé H, Gérentes M-F, Creff A, Thévenin J, Dubreucq B, Ingram GC, Rogowsky PM, and Depège-Fargeix, N.
ZmZHOUPI, an endosperm-specific bHLH transcription factor involved in maize seed development.
Plant J. 2015 [PMID: 26361885]

"Sosso D, Luo D, Li QB, Sasse J, Yang J,...". (2015)
Sosso D, Luo D, Li QB, Sasse J, Yang J, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS, Rogowsky PM, Ross-Ibarra J, Yang B, Frommer WB.
Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport.
Nat Genet. 2015 [PMID: 26523777]

"Rousseau D*, Widiez T*, Di Tommaso S, Rositi...". (2015)
Rousseau D*, Widiez T*, Di Tommaso S, Rositi H, Adrien J, Maire E, Langer M, Olivier C, Peyrin F, Rogowsky P.
Fast virtual histology using X-ray in-line phase tomography: application to the 3D anatomy of maize developing seeds.
Plant Methods. 2015 [PMID:26688690]

2014


"San-Bento R, Farcot E, Galletti R, Creff A,...". (2014)
San-Bento R, Farcot E, Galletti R, Creff A, Ingram G.
Epidermal identity is maintained by cell-cell communication via a universally active feedback-loop in Arabidopsis thaliana. Plant Journal [PMID: 24147836]

"Denay G, Creff A, Moussu S, Wagnon P, Thévenin...". (2014)
Denay G, Creff A, Moussu S, Wagnon P, Thévenin J, Gérentes MF, Chambrier P, Dubreucq B, Ingram G.
Endosperm breakdown in Arabidopsis requires heterodimers of the basic helix-loop-helix proteins ZHOUPI and INDUCER OF CBP EXPRESSION Development. 2014 [PMID: 24553285]

"Smolarkiewicz M, Skrzypczak T, Michalak M,...". (2014)
Smolarkiewicz M, Skrzypczak T, Michalak M, Leśniewicz K, Walker JR, Ingram G, Wojtaszek P.
Gamma-secretase subunits associate in intracellular membrane compartments in Arabidopsis thaliana. J Exp Bot. 2014 [PMID:24723404]

2013


"Waters, A., Creff, A., Goodrich, J., and...". (2013)
Waters, A., Creff, A., Goodrich, J., and Ingram, G. (2013). "What we’ve got here is failure to communicate": Zou mutants and endosperm cell death in seed development. Plant Signal Behav.

"Xing, Q., Creff, A., Waters, A., Tanaka, H.,...". (2013)
Xing, Q., Creff, A., Waters, A., Tanaka, H., Goodrich, J., and Ingram, G.C. (2013). ZHOUPI controls embryonic cuticle formation via a signalling pathway involving the subtilisin protease ABNORMAL LEAF-SHAPE1 and the receptor kinases GASSHO1 and GASSHO2. Development 140, 770-779.

"Moussu S, San-Bento R, Galletti R, Creff A,...". (2013)
Moussu S, San-Bento R, Galletti R, Creff A, Farcot E, Ingram G.
Embryonic cuticle establishment: The great (apoplastic) divide. Plant Signal Behav. 2014 [PMID: 24398513]



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The aim of the Seed Development team is to decipher the molecular mechanisms that govern seed development (embryo, endosperm and seed coat) in the model plant Arabidopsis and the crop plant maize.
Both the embryo and the endosperm undergo a very precise and tightly regulated development from a single cell into a multi-cellular, highly differentiated organism, permanently co-ordinating their growth with that of the other parts of the seed. While the developmental or early phase of seed development is the main interest of the team, the subsequent filling and maturation phases are also of strong interest for us. Independently of the developmental stage, the goals are to identify and characterize the functions of genes important for the seed biology and to generate knowledges for seed breeding that will better fit the demands of a sustainable agriculture.

Current Projects

- Transcriptional regulation of seed development
- Gene network regulated by ZHOUPI in Arabidopsis and maize
- Crosstalks between Seed coat-Endosperm-embryo
- Role of the DEK1 protein in Arabidopsis and maize
- Positional cloning of the gim (gynogenesis) locus in maize
- Maize transformation


Transcriptional regulation of seed development

Cereal seeds are the main source of human nutrition and animal feed throughout the world as well as an important resource for biosourced chemistry and alternative energy production. Therefore, the understanding of seed formation in cereals, and in particular the intimate knowledge of the genes involved, their precise function and their regulation is essential for plant breeding efforts aiming at improving seed yield and quality, stabilising seed traits in fluctuating environments or enhancing industrial uses.
Seeds are complex biological systems composed of three compartments (seed coat, embryo, endosperm) that undergo profound changes during their development characterised by three major stages, i.e. morphogenesis, filling and dehydration. The existence of distinct genetic and epigenetic programs for the three compartments and the three stages of seed development is indicated by transcriptomics analyses in the dicot model species Arabidopsis and several other species.

We now want to address:
- establish maize gene expression patterns at different developmental stages and in different seed compartments on a genome wide basis
- study the conservation in maize of the ABI3/FUS3/LEC2/LEC1 regulatory network, which is essential for seed development in Arabidopsis
- determine the function of specific transcription factors in seed development

Gene network regulated by ZHOUPI in Arabidopsis and maize

One of the major differences between Arabidopsis and maize seeds is the persistence of the endosperm. In Arabidopsis the endosperm is transient, breaking down as the embryo develops to provide space, and possibly nutrients. We have identified The ZHOUPI (ZOU) gene as being required for this process in Arabidopsis. We have also shown that ZOU regulates a signaling pathway which is necessary for the formation of the embryo surface during seed development.
The ZOU protein is conserved in flowering plants and even in club mosses, suggesting that it has an ancient role, possibly regulating the development of the female gametophyte.

We now want to address:
- use transcriptomic approaches to identify downstream targets of ZOU in Arabidopsis, allowing us to pinpoint the processes that usually lead to endosperm breakdown.
- understand the role of ZOU in maize, a plant which naturally has a persistent endosperm. This may teach us more about the ancestral role of ZOU
- unravel the regulatory network surrounding ZOU in both species, by characterization both upstream and co-regulators, and direct targets.

Crosstalks between Seed coat-Endosperm-Embryo

Seed coat (bleu) ; Endosperm (red) ; Embryo (green)
Maize seeds are complex biological systems composed of three compartments: the seed coat (represented in blue on the picture here opposite), the embryo (in green), and its nourishing tissue the endosperm (in red). These tissues undergo profound and tightly synchronize changes during seed development. This emphasizes the necessity to establish communication between these 3 different tissues in order to co-ordinate their developmental programs throughout the seed development. Despite the importance of this communication, how it is achieved remains almost completely unknown.

We now want to address:
- What are the molecular signalling frameworks operating between seed coat, embryo and endosperm tissues?
- What are the effectors of these inter-compartmental signalling pathways?

Role of the DEK1 protein in Arabidopsis and maize

Wild-type cotyledon (left) vs dek1 cotyledon (right)

DEK1 is a highly conserved and essential protein in both Arabidopsis and maize, and is absolutely required for normal cell fate specification in both the developing embryo and endosperm. A preliminary functional dissection of DEK1 has highlighted its extreme importance for growth co-ordination, making it an interesting candidate for a role in inter-tissue and intercompartmental communication during seed development. DEK1 is a complex and big protein that is made of several predicted transmembrane domains and a cytoplasmic tail that includes a calpain protease moiety and a domain of unknown function.

We now want to address the following questions:
- Which are the biochemical functions of the different DEK1 domains? To reach this goal, we are using a wide array of biochemical approaches.
- Why the loss or gain of DEK1 functions results in such extreme and pleiotropic phenotypes? We are currently characterizing in detail the morphological and physiological phenotypes associated with DEK1 activity with the aim of identifying the pathways this protein is involved in.

Positional cloning of the gim (gynogenesis) locus in maize

Gynogenesis (the development of the non-fertilised egg cell into a haploid plant) combined with a colchicine-induced chromosome doubling is nowadays a routine procedure in maize breeding. In maize, it is triggered by the pollination of a plant of interest by a so-called inducer line, and a major QTL of the inducing capacity has been identified on chromosome 1. The objective of the project is the positional cloning of this QTL and the identification of the underlying gene as well as to understand the molecular mechanism involved.

We now want to address:
- determine the exact size of the confidence interval by marker densification
- identify additional recombinants in the interval

Maize transformation


- Maize transformation, technical platform
The role of the platform is to produce transgenic plants that are tools for basic research and are grown exclusively in a confined environment. Created in 2008, the first year of the maize transformation platform was devoted to the establishment of the most widely used maize transformation technique (contact of Agrobacterium with immature embryos) in the team.
The platform is now opened for outside collaborations. For further information please Contact Ghislaine Gendrot

- Improvement of maize transformation
Maize transformation is an essential tool in functional genomics. The currently used standard technique is not very efficient (2 to 5% of the immature embryos put into contact with Agrobacterium tumefaciens are transformed), quite slow (9 months from transformation to T1 seed), limited to a single genotype and labor intensive. The objective of the project is to improve the existing technique and to test innovative transformation tools in maize.
We now want to address:
- establish maize transformation for additional genotypes
- test in planta transformation in maize
- use meganucleases for targeted gene insertion in maize
- use TALEN for gene knockout

Permanent staff
Gwyneth INGRAM DR CNRS +33 4 26 23 39 78
Sophy CHAMOT T CNRS +33 4 72 72 86 14
Audrey CREFF AI CNRS +33 4 72 72 89 85
Nathalie DEPEGE-FARGEIX MdC UCBL +33 4 72 72 89 85
Ghislaine GENDROT AI INRA +33 4 72 72 86 07
Peter ROGOWSKY DR INRA +33 4 72 72 86 07
Thomas WIDIEZ CR INRA +33 4 72 72 86 04
Post-docs & Invited researcher
Pyott DOUGLAS Post-Doc +33 4 26 23 39 78
Anne-Charlotte MARSOLLIER AGPR ENS Lyon +33 4 72 72 89 82
Students
Nicolas DOLL Ph.D student, ENS Lyon (ED BMIC) +33 4 72 72 86 10
Laurine GILLES Ph.D student, ENS Lyon (ED BMIC); CIFRE (CIFRE) +33 4 72 72 39 58
Jeanne LOUE-MANIFEL Ph. D Student, ENS Lyon (ED BMIC) / The University of Edinburgh NA
Angelo GAITI Erasmus Master Student from the University of Milan +33 4 72 72 85 91
Contract staff
Edwige DELAHAYE AI INRA 04 72 72 85 91
Christelle RICHARD AI INRA +33 4 72 72 85 91

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